Behavioral-attentional syndrome following bilateral ... - Springer Link

J Neurol (1998) 245 : 322–324 © Springer-Verlag 1998

S. Canavero M. Fontanella

Behavioral-attentional syndrome following bilateral caudate head ischaemia Received: 24 October 1997 Received in revised form: 12 January 1998 Accepted: 2 February 1998

Sirs: There is growing evidence of an important role of parts of the basal ganglia in cognition and behaviour [1, 8]. Specifically, lesions of the caudate nucleus cause a behavioural disorder more often than a motor disorder (in a ratio of about 4:1), while there is almost no behavioural derangement following putaminal lesions and a two-fold prevalence of motor derangement following pallidal lesions [8]. The caudate nuclei are implicated in the genesis of obsessive-compulsive disorder [11]. However, the exact role thereof remains to be elucidated. Our experience with a patient with bilateral caudate head ischaemia is reported. Only three other as detailed cases have been found in the literature [1, 6]. Prior to her illness, this righthanded 40-year-old woman led a normal life as housewife. No psychiatric or neurological derangement was reported. She was admitted to our ward for a bleeding anterior communicating artery aneurysm. Severe neck stiffness was the only clinical finding. Computed tomography (CT) showed diffuse subarachnoid haemorrhage plus mild intraventricular bleeding; no ischaemic lesions were seen. The aneurysm was clipped through a right pterional approach within 24 h of bleeding. The procedure required no hypotension or temporary clipping. During dissection, a small artery originating from the A2 segment about 6 mm distally from the right A1–A2 junc-

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tion, was coagulated after clipping; since no Heubner artery (i.e. the main feeder to the caudate head) was visible, this was deemed with hindsight to be the main supply to the caudate nuclei. Postoperatively, the patient was conscious and alert, with no gross neurological deficit. CT 3 days later disclosed bilateral ischaemia of the heads of the caudate nuclei, minimal involvement of one putamen and of the anterior limb of the internal capsule and no sign of frontal lobe ischaemia (Fig. 1, left). Following discharge, personality was greatly changed with altered affect, motivation and self-care. Eight months after surgery, neuropsychological assessment (CBA 2.0 Battery) evaluated her intelligence (Wechsler Intelligence Scale, verbal and arithmethical judgement, Raven progressive matrices 38), memory (Wechsler Memory Scale, word span, Corsi spatial span, list learning, spatial learning, prospective memory), language (sentence construction), frontal lobe functions (visual search, Elithorn’s perceptual maze test, planning task, verbal fluencycategory, phonemic, associative, Wisconsin card sorting test). All values were within normal ranges, except for prospective memory (time: 33 vs 96.8 of controls, event: 0 vs 98.6 of controls), planning task (goals: normal, goals and moves: 140 vs less than 87.7 for controls) and the Wisconsin card sorting test. She showed trait-anxiety, disproportionate anxious reactions to nonmenacing situations that she perceived as menacing (Scale 3/STAI X-2), aloofness in interpersonal ties, indifference and, at times, aggressiveness (Scale 5/EPQ/R-P) and an inclination to depression (Scale 8/AD). Scale 9 (MOCQ/R-3) was at the higher range of values, revealing intrusive thoughts, ruminations and doubts on trifles. Globally, the patient showed lack of concern for housework, shopping, personal hy-

giene, sexuality and, in general, her problems and those of her relatives (unlike her previous behaviour). She would spend most of her daytime loafing, watching television until somebody else turned it off, and playing solitaire with stereotyped movements and much in the same way in all sessions. At times, she would compulsively touch objects and people, or express depressive thoughts and cry inappropriately. Her appetite was increased and she gained 35 kg for this reason. She also had difficulty in falling asleep. Magnetic resonance imaging (MRI) 10 months postoperatively confirmed previous CT findings (Fig. 1, right). Single photon emission computed tomography (SPECT) (see [3] for technique description) disclosed broad areas of absence of cerebral blood flow, particularly in basal sectors, and a global cerebral blood flow abatement (Fig. 2): these alterations could not be ascribed to surgical trauma, as no sign of diffuse ischaemia was noted on MRI. The patient was neuropsychologically unchanged at the last follow-up. The prefrontal association cortex projects massively to the caudate nuclei (and very little to the putamen) in an orderly fashion; projections from the orbitofrontal and anterior cingulate cortex target the striosomes, those from the lateral prefrontal convexity target the matrisomes, and the rest (from the limbic areas such as the amygdala) target the matrix [4, 11]. Central to the functional spectrum of the caudate nuclei are the so-called tonically active neurons (TANs), specialized cells that are set to change their firing patterns in response to stimuli that are generally perceived to have behavioural significance (e.g. rewarding stimuli): placed at the matrisome-striosome border junction, they may help to select and generate new striatal activity patterns in response to the integration of behaviourally

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Fig. 1 Left: Computed tomography (CT) scan 3 days after aneurysm surgery shows bilateral caudate head ischaemia, with some involvement of the abutting internal capsule and minimal damage to the putamen. Right: Magnetic resonance image 10 months after surgery confirms previous CT findings

Fig. 2 HMPAO single photon emission computed tomography shows areas of absence of blood flow in the frontal lobes (arrows), somewhat more pronounced on the side of surgical approach (right). The rest of the frontal lobes is subperfused. In view of unrevealing magnetic resonance imaging findings, blood flow alteration would result from diaschisis following caudate ablation; it may also mark a disturbance in the functional organization of on-line frontal activity

significant information [11]. The caudate head would act as a filter or a switch among parallel circuits originating from the frontal cortex. This is in line with recent speculations on the role of the basal ganglia in motricity. According to one such hypothesis [9], the basal ganglia do not generate movement. When voluntary movement is generated by cortical and cerebellar mechanisms, the basal ganglia act broadly to inhibit competing motor programmes that would otherwise interfere with the desired movement. Simultaneously, inhibition is removed focally from the desired motor mechanisms to allow the movement to proceed. In this context, the caudate nuclei would not generate behavioural or cognitive programmes, but merely lock and unlock distinct, discrete circuits from and to the frontal lobes, harmonizing the intended output. Our patient was impaired on the Wisconsin card-sorting test: this involves both the temporary storage of information in a phonological store and the shifting of attention to move information in and out of this score [5]. Impairment implies the inability to switch attention owing to an inability to update the feedback information in the phonological store, with ensuing perseverations. Thus,

the Central Executive or Attentional Allocation System therorized as the basis of frontal lobe function (reviewed in [7]) cannot update information in the temporary stores, particularly if there is more than one chunk of information to be maintained in the working memory (recall our patient’s deficit in the prospective memory task). The caudate heads may integrate the attentional axis (anterior cingulate) and the planning and behavioural axis (dorsolateral cortex). The dorsolateral prefrontal cortex is crucial for integrating information from all three main frontal association circuits (dorsolateral/orbitofrontal/medial frontal) that can be acted upon through the executive motor circuitry [4]. Thus, caudate head disruption could be expected to result in flat affect and aloofness, owing to attentional deficit (rewarding stimuli cannot be appreciated), and perseverations (e.g. hyperphagia, hypersomnia, compulsive touch). Other signs would include deficits in complex calculations and comprehension of complex ideational material [10]. This is a “lock-unlock” syndrome and explains the existence of simultaneous abnormal behaviour and inhibition behaviour. Some features are

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those of the syndrome of loss of psychic self-activation [2]. In conclusion, the caudate heads do seem to play a paramount role in the integraion of behaviour. References 1. Bhatia KP, Marsden CD (1994) The behavioual and motor consequences of focal lesions of the basal ganglia in man. Brain 117:859–876 2. Bogousslavsky J (1994) Frontal stroke syndromes. Eur Neurol 34:306–315 3. Canavero S, Pagni CA, Castellano G, Bonicalzi V, Bello’ M, Duca S, Podio V (1993) The role of cortex in central pain syndromes: preliminary results of a long-term Tc99-hexamethylpropyleneamineoxime single photon emission computed tomography study. Neurosurgery 32:185–191

4. Cummings JL (1995) Anatomic and behavioral aspects of frontal-subcortical circuits. In: Grafman J, Holyoak KJ, Boller F (eds) Structure and function of the human prefrontal cortex. Ann N Y Acad Sci 769:1–14 5. Dunbar K, Sussman D (1995) Toward a cognitive account of frontal lobe function: simulating frontal lobe deficits in normal subjects. In: Grafman J, Holyoak KJ, Boller F (eds) Structure and function of the human prefrontal cortex. Ann N Y Acad Sci 769:289–304 6. Fukamachi A, Horikoshi T, Nagaseki Y, Sasaki H, Nukut H (1987) Symmetrical bilateral low-density lesions in the area of supply by Heuner’s arteries after aneurysm surgery. Acta Neurochir (Wien) 84:89–92 7. Grafman J, Holyoak KJ, Boller F (eds) (1995) Structure and function of the human prefrontal cortex. Ann N Y Acad Sci 769:289–304 8. Middleton FA, Strick PL (1994) Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. Science 266:458– 461

9. Mink JW (1996) The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 50:381–425 10. Richfield EK, Twyman R, Berent S (1987) Neurological syndrome following bilateral damage to the head of the caudate nuclei. Ann Neurol 22:768– 771 11. Schwarz JM (1997) Obsessive-compulsive disorder. Sci Med 2:14–23 S. Canavero · M. Fontanella Functional and vascular surgery branches, Department of Neurosciences, Molinette Hospital, Turin, Italy S. Canavero (Y) Via Montomagno 46, I-10132 Torino, Italy