ERP indexes of functional differences in brain

Neuropsychologia 39 (2001) 815– 827 www.elsevier.com/locate/neuropsychologia

ERP indexes of functional differences in brain activation during proper and common names retrieval Alice Mado Proverbio a,*, Stefania Lilli a, Carlo Semenza a, Alberto Zani b b

a Department of Psychology, Uni6ersity of Trieste, Via S.Anastasio 12, 34134 Trieste, Italy Istituto di Neuroscienze e Bioimmagini, Consiglio Nazionale delle Ricerche, Via Fratelli Cer6i 93, 20090 Segrate, Milano, Italy

Received 14 July 1998; received in revised form 23 November 2000; accepted 1 December 2000

Abstract Functional neuroimaging and neuropsychological findings suggest that memory retrieval of common and proper names is subserved by different neuro-functional systems but little is known about the topographic localization of neural generators. In the present study brain electrical activity was recorded with a high density electrode montage in healthy young volunteers during lexical retrieval upon written definition. ERPs spatio-temporal mapping showed on one side a strong activation of left anterior temporal and left central-frontal areas for proper names, and on the other side a greater involvement of occipital areas for common names retrieval. The specific pattern of bio-electrical activity recorded during proper names retrieval might index the activation of neural circuits for recalling names of high contextual complexity, poor of sensory– motor associations and dependent on precise spatio-temporal coordinates. © 2001 Elsevier Science Ltd. All rights reserved. Keywords: ERPs; Memory retrieval; Lexical category; Left temporal lobe; Phonological decision

1. Introduction Common names refer to entities belonging to a category of non-unique individuals (such as animals, vegetables, tools) described by their functional and semantic properties, whereas proper names refer to unique individuals (persons, places) dependent on a very high level of contextual complexity for their definition and with a one-to-one relationship with their referents. This difference has been argued to require different retrieval processes, perhaps more sourcedemanding in the case of proper names [5,34,40]. Recent neuropsychological observations have supported such claim, suggesting that functional differences may be matched by the working of separate neural mechanisms devoted to the retrieval of the two name categories [37].

The present work has been carried out at the Lab of Cognitive Electrophysiology of Department of Psychology, University of Trieste. * Corresponding author. Tel.: + 39-40-6762730; fax: + 39-404528022. E-mail address: [email protected] (A.M. Proverbio).

Patients suffering from proper name anomia have been described as being selectively unable to name any persons (even relatives and friends) or geographical sites on visual confrontation or from definition, without showing any deficit in the ability to pronounce the words or comprehend their conceptual meaning, as well as to name words of any other category [22,26,37]. Selective sparing of proper name production has also been reported [4,36]. Interestingly, proper name comprehension can be preserved even when common-name comprehension is severely impaired [25,42]. The neuropsychological literature describes other kinds of patients suffering from color anomia who are selectively unable to put names to colors, although being perfectly capable of matching the visual representation of an object (for example, a banana) with its prototypical color [7]. Similar dissociations have been found for other categories like living vs. non-living entities [27,38]. Overall, the deficit seems to be restricted to the ability to name or retrieve lexical units without affecting comprehension processes. However, the precise identification of the brain areas endowing such mechanisms is still matter of debate [6,8,28,35]. For example, selective deficits in the ability to retrieve

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A.M. Pro6erbio et al. / Neuropsychologia 39 (2001) 815–827

Table 1 Examples of unique definitions of three proper and common names selected on the basis of the following parametersa,b Unique definition

Name

FREQ

SCORE

LET

SYL

Headquarters town of Fiat Opera theatre in Milan Leader of Forza Italia party

Proper Torino La Scala Berlusconi

18 12 1

4 4 3

6 7 10

3 3 4

Boundary between two countries Opens a lock Collects and sells old furnitures

Common (border) confine (key) chiave (antiquarian) antiquario

18 12 1

4 4 3

7 6 10

3 2 4

a FREQ, word frequency (according to De Mauro et al. [10]); LET, numbers of letters; SYL, numbers of syllables; SCORE, ease of retrieval (from −4 to +4, according to a questionnaire previously administered to 40 subjects in a pilot study). b Items of balanced scores were chosen from a larger initial sample.

proper names have been described as a consequence of left temporal lobectomy [16], left medial and lateral temporal lobe damage [32], left temporal lobe atrophy [11], and mild left cerebral atrophy [13]. The PET study by Gorno Tempini et al. [19] have shown a greater activation of the left lateral anterior middle temporal cortex to famous names than to common object names in normal individuals during a categorization task. Again, the combined PET and neurological study by Damasio et al. [7] found that the retrieval of person, animal and tool names in a naming task depended on the activation of three distinct regions of the left temporal lobe, namely: temporal pole, infero-temporal and posterior temporal. These data, although certainly of remarkable value for localizing lexical access for different name categories, only indirectly measured brain activation involved in retrieval processes because of the particular tasks adopted (i.e. categorization and naming). In this kind of paradigms, brain activity recorded during task performance necessarily reflects the different mental processes required by it, namely reading and comprehension, memory retrieval and naming. In order to avoid this shortcoming we developed an original paradigm in which the retrieval task temporally preceded a secondary non-simultaneous task in which participants were engaged. Our task consisted in silently retrieving names upon written definition in order to perform a phonological decision task. EEG was recorded during the retrieval process by triggering it to a neutral visual probe (a question mark), which was then followed by a linguistic target. Aim of the present study was to gain further knowledge on brain mechanisms involved in lexical retrieval by directly measuring the spatio-temporal dynamics of brain activation as indexed by event-related potentials (ERPs) during proper vs. common names memory recall. The secondary task was introduced to ensure that subjects were retrieving the defined words, and to force them to do it in a given time having actually access to the complete graphemic and phonological form of

names. This original paradigm was designed also to reduce the inter-trials variability (thus preventing the incomplete retrieval typical of ‘tip of the tongue’ phenomena) and to control for losses of concentration or memory lacks, given that participants were compelled to make a decision and perform a motor output as fast and accurately as possible on the base of the retrieved name. One possible shortcoming of the present paradigm is that is relatively impossible to establish for each single item at which point of memory retrieval processes the ERPs were recorded. Furthermore, it has to be considered that, although the retrieval of each specific name could begin only when the sentence reading was almost completed, a certain activation of a given semantic context gradually took place during the sentence reading. However, by averaging together several thousands of probe-locked epochs (across trials and subjects), we were able to measure brain activation during memory retrieval of proper and common names, independent of other parameters (difficulty of retrieval, length, frequency, etc). On the other hand, one of the most valuable aspect of this paradigm is that allows to measure brain potentials related to memory retrieval without engaging the

Fig. 1. Sketch of the experimental procedure on a time scale. The first arrow indicates the onset of ERP recording.


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Fig. 2. Mean reaction times (RTs) to trigrams and percentages of error made by participants in the phonological decision task as a function of name category and inclusion in the target name. Overall, there was a slight advantage for the decision involving common names.

observers in complex visual or linguistic processing, by adopting a meaningless not-interfering probe to timelock ERPs.

2. Methods

2.1. Subjects Nine right-handed university students (4 males, 5 females) with a mean age of 26 years participated in our experiment. All were native Italian speakers and had normal or corrected-to-normal vision.

2.2. Stimuli and procedure A set of 332 items (166 common and 166 proper names) were adopted as target names (i.e. names to be retrieved, see Appendix A and Appendix B, respectively). They were balanced for length, number of syllables, phonological complexity, and word frequency. The ease of retrieval was also carefully balanced across proper and common names, by administering a questionnaire with hundreds of written definitions to a sample of 40 college students of same age and asking them to retrieve the defined items within 2 s, write down the answer and judge the difficulty of recalling each item with a 5 points scale (from very difficult to very easy). As a result of the data obtained in this preliminary test only a portion of the initial set of 490 definitions was judged suitable to be adopted. Selected stimuli had a high or medium facility of retrieval, and were perfectly balanced across the two lexical categories for facility of retrieval and frequency of use, besides the other standard parameters (see examples of matched definitions in Table 1). Nouns of different imagery value (abstract and concrete names) were included in common names category. Three hundred and thirty-

two different 3-letters syllables were selected for the phonological decision task. Half of them were included in the target words at the beginning, in the middle, or in the final part. Their pronunciation was the same whether in isolation or within the word. The task consisted in silently retrieving names upon written definition in order to perform a phonological decision task (see Fig. 1). Participants seated in a dimly lit, acoustically and electrically shielded box at 114 cm from a TV screen. They were instructed to fixate a cross at the center of the screen and read a short definition which appeared for 2 s in the upper part of the central visual field. After 500 ms a question mark, which was used as a probe, was presented at the center of the screen for 750–1000 ms, and substituted right after by a trigram presented for 200 ms. Participants were instructed to retrieve the target names, and to decide thereafter whether the syllable was part of the target by pressing as accurately

Fig. 3. Grand-average ERP waveforms recorded at left (T3) and right (T4) temporal sites during proper and common names retrieval. Note the greater N1 and P3 amplitude values (in mV) elicited by proper names recalling over the left hemisphere.


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Table 2 Significance levels of analyses of variance for each ERP component considereda,b Component

Amplitude N1 occipital

N1 temporal N2 P270–320 P350–430

P270–320 midline P350–430 midline Latency N1 occipital N2

Factor

Significance level

m

Corrected P-values

E E×H N×E×H N×H E N×E E E×H E H N×H E×H N×E×H N

PB0.02 PB0.005 PB0.04 PB0.03 PB0.0035 PB0.02 PB0.01 PB0.0035 PB0.005 PB0.006 P=0.08 PB0.0007 PB0.035 P= 0.056

0.57 0.63 0.70 1 0.93 0.66 0.64 0.64 0.40 1 1 0.53 0.77 1

0.03 0.01 0.05 PB0.03 PB0.0035 0.05 0.05 0.01 0.05 PB0.006 P= 0.08 0.02 0.05 P= 0.056

N

PB0.03

1

PB0.03

H E×H N E

PB0.009 PB0.005 PB0.045 PB0.04

1 0.68 1 0.92

PB0.009 0.02 PB0.045 PB0.04

a

E, Electrode; H, Hemisphere; N, Lexical category. Reported P-values are corrected on the basis of the Greenhouse– Geisser epsilon (m) adjustment for repeated measure designs whenever the latter was less than 0.85. b

and fast as possible a button with the index finger for answer ‘yes’, and another one with the medium finger for the answer ‘no’. The two hands were used alternatively during the recording session and the hand order was counterbalanced across subjects. The electroencephalogram (EEG) was continuously recorded from 28 scalp sites using tin electrodes mounted in an elastic cap (Electro-cap, Inc.). The electrodes were located at frontal (Fp1, Fp2, FZ, F3, F4, F7, F8), central (CZ, C3, C4), temporal (T3, T4), posterior temporal (T5, T6), parietal (PZ, P3, P4), and occipital scalp sites (OZ, O1, O2) of the International 10– 20 System. Additional electrodes were placed half the distance between anterior temporal and central sites (FTC1, FTC2), central and parietal sites (CP1, CP2), anterior temporal and parietal sites (TCP1, TCP2), and posterior temporal and occipital sites (OL, OR). Blinks and vertical eye movements (i.e. EOG) were monitored by means of two electrodes placed below and above the right eye, while horizontal movements were recorded from electrodes placed at the outer canthi of the eyes. Average ears served as reference lead. The EEG and the EOG were amplified with a half-amplitude band pass of 0.1–70 and 0.01– 70 Hz, respectively. Electrode impedance was kept below 5 kV. Continuous EEG and EOG

were digitized at a rate of 512 samples per second. Computerized artifact rejection was performed before averaging to discard epochs in which eye movements, blinks, excessive muscle potentials or amplifier blocking occurred. Artifact rejection criteria was: peak to peak amplitude exceeding 950 mV. The artifact rejection rate was about 5%. ERPs were averaged offline from 100 ms before to 1000 after probe presentation. ERP trials associated with an incorrect behavioral response were excluded from further analysis. For each subject, distinct ERP averages were obtained as a function of name category. The major ERP components were identified and measured automatically by a computer program with reference to the baseline voltage averages over the interval from 100 to 0 ms. ERP components were labeled according to a polarity– latency convention and quantified by measuring peak latency and baseline-to-peak amplitude values within a specific latency range centered approximately on the peak latency of the deflection seen in the grand average waveforms. Temporal N1 component peaking at about 150 ms was defined as the most negative deflection among 120–180 ms at T3 and T4 sites. Occipital N1 component, peaking at about 185 ms, was defined as the most negative deflection among 150 and 215 ms at homologous O1 –O2, OL –OR, T5 –T6, P3 –P4 electrode sites. Posterior N2 component, peaking at about 275 ms, was defined as the most negative deflection among 250–305 ms at homologous O1–O2, OL –OR, and T5 –T6 electrodes. Furthermore, two major late positive deflections were identified in the P300 latency range among 270–320 and 350–430 ms, respectively, at F3–F4, F7 –F8, C3 –C4, P3 –P4, CP1 –CP2, TCP1 –TCP2, FTC1 –FTC2 electrode sites. ERP amplitude and latency measures were analyzed with repeated-measure analyses of variance (ANOVAs), separately for each ERP component. Factors were ‘name category’ (proper and common), ‘electrode site’ (depending on the ERP component of interest) and ‘cerebral hemisphere’. Greenhouse –Geisser corrections were employed to reduce the positive bias resulting from repeated factors with greater than two levels. Post-hoc Tukey test was carried out for multiple mean comparisons. Topographical voltage maps of ERP components were obtained by plotting color-coded iso-potential contour lines derived by interpolation of voltage values between scalp electrodes at specific latencies. For each subject errors and misses percentages were transformed in arcsin values and submitted to a two way ANOVA. Reaction times to trigrams not exceeding 2 standard deviations above or below the mean were also submitted to a two way ANOVA. Factors were ‘name category’ (proper and common) and inclusion (being included or not in the target name).


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Fig. 4. Isocontour voltage maps of brain activation obtained by subtracting neural activity related to common from that related to proper names in the N1 latency range. Note that the left and right sides correspond to the left and right hemispheres of the brain, respectively. The blue focus indicates a greater activation of left anterior temporal/inferior frontal regions for proper names retrieval.

3. Results

3.1. Beha6ioral results Fig. 2 shows reaction times and percentages of error made by participants in the decision task. Frequency of correct responses was about 85%. Participants committed slightly more errors in deciding about proper than common names (F1, 8=7.31; P B0.03) as proved by the significant effect of lexical category (see the data displayed on the left side of Fig. 2). Also, errors tended to be fewer when the syllables were not part of the target name, thus suggesting that they were not used to evoke afterwards the target word by visually priming it. Responses were on average 25 ms faster to common than proper names, as confirmed by the significance of name category effect (F1, 8=16.37; P B0.004).

3.2. Electrophysiological results ERPs to the probe were characterized by a series of negative deflections asymmetrically distributed over the

left hemisphere. In particular, the anterior portion of the left temporal lobe was selectively activated by proper name retrieval about 150 ms after the probe (see Table 3 Mean amplitude values of temporal N150 as a function of lexical category and cerebral hemisphere Temporal N150

T3

T4

Common Proper Tukey test

0.73 −1.51 0.05

−0.68 −0.95 n.s.

Table 4 Mean latency values of occipital N186 as a function of electrode site and cerebral hemisphere Occipital N186

Parietal

Occipital

Posterior temporal

Latency occipital

Left Right Tukey test

187 193 0.01

185 188 –

178 189 0.01

180 188 0.01


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Table 5 Mean amplitude values of occipital N186 as a function of lexical category, electrode site and cerebral hemisphere Occipital N186

P3

P4

O1

O2

T5

T6

OL

OR

Common Proper Tukey test

−1.99 −2.18 −0.01

−3.09 −3.66 −0.01

−3.95 −3.83 –

−3.33 −3.28 –

−4.91 −4.73 –

−4.64 −5.03 0.01

−5.52 −5.25 –

−4.95 −5.13 –

waveforms of Fig. 3). The ANOVA carried out on mean amplitude values of temporal N1 component revealed the significant interaction of ‘lexical category’ × ‘hemisphere’ (F1, 8=6.63; P B 0.03) which statistically confirmed this hemispheric asymmetry specific to proper names at temporal sites (see Table 2 for a summary of statistical significances). While N1 to common names did not differ in amplitude as a function of cerebral hemisphere, N1 to proper names was larger on the left than right hemisphere (Tukey posthoc comparison: PB0.01) as depicted in brain maps of Fig. 4. Furthermore it was much larger to proper than common names only at the left hemispheric site, as confirmed by post-hoc comparisons (see means and significance in Table 3). Fig. 4 shows voltage maps of brain activation related to proper names retrieval, obtained by subtracting neural activity to common from that related to proper names at the peak latency of temporal N1 (about 150 ms post-stimulus). These maps show a maximum distribution of negativity at the left temporal side. The ANOVA performed on mean latency values of N1 occipital component showed that it was earlier at left (182 ms) than right hemispheric sites (190 ms), as indicated by the significance of factor ‘hemisphere’ (F1, 8=11.9; PB 0.009). The ANOVA also showed a significant interaction of ‘electrode’ × ‘hemisphere’ (F3, 24= 5.6; P B0.005), indicating that this negative component was earlier at left than right posterior-temporal, lateral-temporal and lateral-occipital sites (see Table 4 for post-hoc comparisons). As for the amplitude measures, a main effect of electrode was found (F3, 24=4.55; P B 0.02) indicating larger amplitudes of posterior N1 at lateral occipital and posterior temporal sites, compared to mesial occipital and parietal sites, as confirmed by post-hoc comparisons (P B 0.01). The significant interaction of ‘electrode’ ×‘hemisphere’ (F3, 24= 5.6, P \ 0.005) showed that this component was larger over the right hemisphere at parietal sites (P \0.01), whereas no hemispheric asymmetry was found for N1 amplitude at other electrode sites. More interesting for the purpose of our investigation was the triple significant interaction of ‘name’ ×‘electrode’ × ‘hemisphere’ (F3, 24= 3.21, P B 0.05) showing an effect of name category, in that N1 was larger for proper than common names at right parietal and posterior temporal sites (see means and post-hoc significances in Table 5).

The ANOVA performed on latency measures of later posterior component N275 showed that it was earlier at mesial electrode sites (‘electrode’ factor: F1, 8=4; PB 0.05), and to common (270 ms) than proper (279 ms) names (‘name category’ factor: F1, 8= 5.6; P B0.05). The ANOVA performed on amplitude measures of the same component gave rise to the significant interaction of ‘name category’ × ‘electrode site’ (F2, 16= 5.2; PB 0.02) indicating that this negative deflection was larger to common (− 1.15 mV) than proper (− 0.06 mV) names at mesial-occipital electrode sites (as confirmed by post-hoc comparisons between means: PB 0.01). In summary, common names retrieval produced a stronger activation of visual cortex after about 250 ms of latency (see waveforms of Fig. 5). Maps of Fig. 6 show the topographical distribution of brain activation recorded during common and proper names in the N2 latency range. It is possible to see a stronger negative focus at mesial electrode sites and a broader voltage distribution over occipital areas during retrieval of common names. This involvement of visual areas may be related to the greater imagery value of common names whose recall may activate a larger amount of sensory–visual associations.

Fig. 5. Grand-average ERP waveforms recorded at posterior electrode sites during memory retrieval of common and proper names. Electrodes were located at homologous temporal (T3, T4), posterior temporal (T5, T6), lateral occipital (OL, OR), and mesial occipital (O1, O2) electrode sites of the left and right hemispheres.


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Fig. 6. Isocontour voltage maps of brain activation recorded during common (top) and proper names (bottom) retrieval in the N2 latency range (260– 280 ms). Note that the left and right sides correspond to the left and right hemispheres of the brain. The blue bilateral foci indicate a greater activation of visual areas for common names retrieval, with an involvement of parietal and lateral occipital areas.

The N2 posterior negative deflection was followed by a large positivity (P300) which showed multiple foci (see waveforms of Fig. 7). An earlier positive deflection (270–320 ms), peaking at about 307 ms, was larger at the right than left parietal site, as indicated by post-hoc comparisons (P B0.05) computed for the significant interaction of ‘electrode’ × ‘hemisphere’ (F6, 48= 2.9; P B0.02), and did not differ in amplitude as a function of name category. A later positive deflection (350–430), peaking at about 390 ms, was much larger to proper than common names, this difference being more pronounced over left centro-parietal sites (see Fig. 8a and b) as confirmed by statistical significance of ‘electrode site’ × ‘name category’ ×‘hemisphere’ (F6, 48=2.5; PB 0.035) and relative post-hoc comparisons (see significances in Table 6). Fig. 9 shows topographical mapping of P300 voltage obtained by subtracting the response related to common from that to proper names retrieval. Bright colors indicate the maximum distribution of positivity related to proper names retrieval. The analysis of voltage distribution revealed that right hemispheric sites were not much sensitive to lexical categories. Indeed, proper

Fig. 7. Grand-average ERP waveforms recorded at anterior electrode sites during memory retrieval of common and proper names. Electrodes were located at homologous frontal (F3, F4), central (C3, C4), central-parietal (Cp1, Cp2), and parietal (P3, P4) electrode sites of the left and right hemispheres.


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proper 3.91 mV) than the second processing phase (F1, 8= 6.58, PB 0.04; common, 3.13 mV; proper 4.98 mV).

4. Discussion

Fig. 8. (a) P390 mean amplitude values recorded at anterior electrode sites of the left hemisphere. The figure shows a much greater P3 response to proper (dashed line) than common names (solid line) over the central-parietal area, confirmed by statistical analyses. (b) P390 mean amplitude values recorded at anterior electrode sites of the right hemisphere. At these sites P3 response did not differ significantly as a function of lexical category. Legend as from Fig. 8a.

names retrieval was characterized by a left temporal and centro-parietal activation followed by the involvement of left prefrontal and central areas. Additional ANOVAs were carried out for P300 values recorded at midline sites Cz, Fz and Pz in the two latency ranges of 270– 320 and 350– 430 ms. P300 amplitude was affected by lexical category in both temporal windows, although the effect was much smaller in the first (F1, 8=4.97, P= 0.056; common, 3.60 mV;

Numerous PET and ERP studies have demonstrated a differential activation of multiple brain regions during processing of words belonging to different lexical categories [6,9,15,23,24,28–31,41]. For instance, the ERPs study by Dehaene [6] have shown the specific activation of left inferior temporal area for proper names, as opposed to a left temporo-parietal activity for animal names and verbs, and a bilateral activation for numerals in a semantic categorization task. The loci of ERP activation found in the present study provided us with a complex pattern of brain activation probably related to lexical access and memory retrieval processes for proper vs. common names. Overall, the specific pattern of bioelectrical activity recorded during retrieval of proper vs. common names might index the activation of partially overlapping cortical regions differentially involved in memory retrieval because of specific properties of the two lexical categories. Common names retrieval was characterized by a stronger activation of visual areas in the N2 latency range. This result might be interpreted in terms of a greater amount of visual–sensory associations linked to common rather than proper names. Indeed, common names generally apply to items described in terms of visual and semantic properties (e.g. objects, tools, animals, body parts, etc.), whereas proper names would work as ‘pure referring expressions’ [37] without describing any attribute properties of the corresponding entity (e.g. persons or geographical sites). A similar interpretation of neural activation dependent on functional properties of lexical items has been claimed to account for the finding that animal names activate more posterior brain regions than tool names [24]. Indeed, tools would be associated with proprioceptive sensations and particular hand motoric patterns due to their manipulability, whereas concrete objects would be associated with a greater amount of visual representations. In addition, verbs, which are known to activate more anterior brain regions compared to nouns [9,29,31], would be linked to sensory–motor associa-

Table 6 Significances of the post-hoc comparisons with the Tukey test for P390 mean amplitudes recorded at left hemisphere anterior sites as a function of lexical category, and shown in Fig. 8a Central P390

F7

F3

C3

Cp1

P3

FTCp1

TCp1

Common vs. proper Significance value

–

–

0.01

0.01

0.05

0.01

0.01


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Fig. 9. Isocontour voltage maps of brain activation obtained by subtracting neural activity related to common from that related to proper names in the latency range of the later P3. The left map refers to the rising phase (320 – 370 ms) and the right map to the peak of this component (390 ms). Anterior brain areas appear in the upper portion, and the left and right hemispheres in the left and right sides of the schematic heads shown in top view. Bright colors indicate strong sources of activation specific to proper names retrieval. The voltage scale is the same of Fig. 4.

tions stored in motor and pre-motor brain areas. Recently [30], it has been demonstrated that these results did not depend on grammatical differences alone (i.e. verbs vs. nouns), given that nouns with strong visual associations activated occipital brain regions to a greater extent than nouns with strong action association. It has been suggested that mechanisms of sensory integration may play an important role in establishing the semantic representation of nouns [17]. The greater activation of visual areas reported in the present study, and in particular of mesial occipital sites, may reflect the greater amount of visual– sensory associations activated during common vs. proper names retrieval. This hypothesis is supported by several neuroimaging studies which investigated brain activation during visual imagery. Several PET studies have documented an activation of visual cortex (area 17 [21] and areas 18 and 19 [20]) in persons with close eyes while they were engaged in visualizing objects of different size and properties. The single photon emission tomography (SPECT) study by Goldenberg et al. [18] reported an increased blood flow in posterior visual areas during imagery. Similarly, electrophysiological data have indicated a greater brain evoked response at posterior scalp sites during visual imagery [12]. Overall, these findings suggest that memory retrieval of common names produce an activation

of visual areas because of their highly depictive semantic representation. In the present study, proper names retrieval yielded a strong activation of the anterior left temporal area, which is broadly consistent with Damasio’s et al. [7] PET finding of an activation of the temporal pole. This consistency suggests the intriguing possibility that the focus of activation we found might reflect the neural activity of the left temporal pole. This correspondence might be supported by the fact that the retrieval of akin material (memory for public events, historical figures and technical terms) has also been found localized in this brain area [43]. It is worth noting that the activation of the left temporal region has also been found during tasks involving episodic memory [33]. All these findings may speculatively be accounted for by the fact that memory for proper names may share at a more peripheral, lexical level, some of the properties that distinguish episodic from semantic memory. Indeed, episodic memory retrieval may be defined as the retrieval of unique information linked to precise spatiotemporal coordinates [39] as opposed to concepts stored in semantic memory, which are independent of any spatial or temporal context. Then, we propose that common and proper names retrieval differentially activates neurofunctional circuits of memory because of their intrinsic properties (i.e. proper names referring to

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unique individuals depending on a high contextual complexity for their definition and common names being linked to strong sensory–motor associations). In this regard, it might be argued that the differential activation dependent on the lexical category is to be attributed tout court to a greater difficulty in retrieving proper names [40]. This interpretation would be somehow supported by our behavioral results (i.e. a slight advantage in retrieving common names), notwithstanding the fact that, in the present study, names belonging to different categories were carefully balanced for ease of retrieval and word frequency. Some support to this hypothesis is also offered by the P300 data showing a greater left prefrontal activation during proper names retrieval. Indeed, the available literature on memory retrieval seems to support the view that, while the right prefrontal region is thought to guide retrieval by indexing the attempt for such recovery, or the ‘retrieval mode’ [2,3], the left prefrontal activation is often associated with difficult retrieval demands and might index the specific effort deployed in the retrieval attempt. In this regard, Backman et al. [1] noted that in most of neuroimaging studies reporting a bilateral prefrontal activation the retrieval demands were greater than in those reporting only a right prefrontal activation. In addition, the left prefrontal area has been also reported to be involved in retrieval of non-imaginable vs. imaginable words [14]. It may be tentatively hypothesized that this brain area, along with the anterior left temporal one, is part of a network activated during retrieval of information dependent on precise spatio-temporal coordinates and poor of sensory associations. These lines of evidence notwithstanding, given the lack of direct knowledge of the intracerebral sources of the various foci of activation found in the present study, further investigations with high spatial resolution neuroimaging techniques would certainly lend stronger support to the assumptions advanced above.

5. Conclusion ERPs high density mapping showed a greater activation of left anterior temporal and left fronto-central sites for proper names, as opposed to a greater involvement of visual areas and a reduced hemispheric asymmetry for common names. The present results are substantially consistent with recent neuroimaging findings in literature. This, in our view, lends support to the robustness of our results notwithstanding the ERP limitations in neural source localization. All in all, we propose that the different pattern of brain activation obtained for the two categories of names may not be simply explained by their belonging to

distinct lexical categories (determining their storage in separate neural loci), but by the specific properties of their semantic organization, characterized by a different pattern of associative links with sensory– motor, linguistic and phonological representations.

Acknowledgements Supported by MURST grants to the Psychology Department of University of Trieste and by a grant from Consiglio Nazionale delle Ricerche to A.Z.

Appendix A. List of common names used as target stimuli in the recall task for each semantic area

Places Ascensore Aula Banca Campagna Campeggio Circo Confine Cucina Duomo Isola Lager Lago Mare Ospedale Piramide Tram Tribunale

Elevator Teaching Room Bank Country Camping Circus Border Kitchen Dome Island Lager Lake Sea Hospital Pyramid Tram Tribunal

Medicine Aborto Afasia Ambulanza Aorta Apnea Arteria Autopsia Barella Balbuzie Bava Cadavere Depressione Emorragia Gas Globulo Mummia Neonato Neurone

Abortion Aphasia Ambulance Aorta Apnoea Artery Autopsy Stretcher Stutter Slobber Corpse Depression Haemorrage Gas Globule Mummy Newborn Neuron


Persons Antiquario Arbitro Calzolaio Ladro Matricola Orfano Papa Pirata Presidente Sosia

Antiquarian Referee Cobbler Thief Freshman Orphan Pope Pirate President Double

Household things Armadio Bicchiere Bilancia Candela Chiave Dentifricio Forno Gomma Grondaia Gesso Gomitolo Lampadario Lavatrice Libro Pianoforte Quadro Sapone Termometro Trapano

Wardrobe Glass Balance Candle Key Toothpaste Oven Eraser Roof gutter Chalk Clew Chandelier Washing Machine Book Piano Painting Soap Thermometer Drill

Animals Anguilla Ape Balena Cammello Canarino Canguro Coccodrillo Dinosauro Elefante Farfalla Gatto Letame Lucciola Maiale Pavone Pidocchio Riccio Rondine Salmone Sanguisuga Scimmia Talpa

Eel Bee Whale Camel Canary Cangaroo Crocodile Dinosaur Elephant Butterfly Cat Manure Firefly Pig Peacock Louse Hedgehog Swallow Salmon Leech Monkey Mole

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Toro Zanzara Zebra

Bull Mosquito Zebra

Abstract nouns, numberals Battesimo Cinque Colazione Costituzione Desiderio Dialetto Digiuno Divieto Due Ergastolo Esilio Fame Incubo Matrimonio Memoria Morte Multa Sciopero Secolo Statura Storia Tennis Verita`

Baptism Five Breakfast Constitution Wish Dialect Fasting Prohibition Two Life sentence Banishment Hunger Nightmare Marriage Memory Death Fine Strike Century Stature History Tennis Truth

Body-parts, garments Guanti Mignolo Mutande Occhiali Ombelico Pigiama Smalto

Gloves Little finger Underpants Spectacles Navel Pajamas Polish

Generic objects Benzina Botte Bullone Chicco Corona Cristallo Cronometro Cubo Diga Flauto Guscio Lana Lapide Nodo Patente Scultura Tarocchi

Gasoline Barrel Bolt Grain Crown Crystal Chronometer Cube Dam Flute Shell Wool Tombstone Knot Driving license Sculpture Tarots


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Eatables Albume Birra Banana Castagna Confetti Limone Miele Mollica Pane Ricino

Albumen Beer Banana Chestnut Sugar-coated almonds Lemon Honey Crumb Bread Castor oil

Natural e6ents, plants Arcobaleno Bora Buio Cipresso Corteccia Cratere Deserto Eclisse Fiume Fulmine Grandine Mimosa Miraggio Neve Nuvola Rosa Stella Tramonto Terremoto

Rainbow Bo`ra Wind Darkness Cypress Bark Crater Desert Eclipse River Lightning Hail Mimosa Mirage Snow Cloud Rose Star Sunset Earthquake

Appendix B. List of proper names used as target stimuli in the recall task for each semantic area Person names Science Binet Broca Kanizsa Korsakov Einstein Lorentz Lumiere Montalcini Morse Pavlov Pitagora Rubbia Skinner Volta Wundt

History Attila Caino Cleopatra Colombo Garibaldi Ghandi Giuda Guelfi Hitler Kennedy Khomeini Marx Mussolini Noe` Mose`

Nerone Nostradamus Pilato Remo Stalin Tito Literature, music Ariosto Beethoven Celentano Dalla Eco Foscolo Goldoni Manzoni

Modugno Mozart Omero Pavarotti Ricciarelli Strauss Verga Verne Vivaldi Cinema, TV Angela Astair Bardot Barbato Basinger Benigni Campbell Castagna Chaplin Fellini Fiorello Monroe Onlio Rame Schiffer Spielberg Stallone Troisi Verdone Villaggio Politics Agnelli Andreotti Berlusconi Bossi Clinton Craxi Diana Illy Moro Pannella Reagan Scalfaro

Fiction, Mithology Aladino Arlecchino Beatrice Befana Biancaneve Caronte Cenerentola Derrick Francesco (St.) Khalı` Giulietta Giuseppe (St.) Pinocchio Stefano (St.) Silvestro (St.) Titanic Valentino(St.) Venere Sport Maradona Meissner Moser Panatta Tomba Geographical names Adriatico Africa Argentina Arno Australia Berlino Bermuda Brasile Campania Carnia Cattinara Capri Cernobyl Dover Egitto

Eiffel Etna Firenze Gibilterra Milano Miramare Monza Mosca Murano Napoli Olanda Opicina Palmanova Pasqua Pirenei Pisa Pompei Po Puglia Roma Romagna Saturno Senna Sicilia Spagna Sparta Tamigi Tevere Torino Venezia Verona Vesuvio Vienna Yugoslavia Various Bayer Disney Kasparov La Scala Marlboro McDonald Onassis Oscar (Prize) Polaroid

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