The effect of anterior thalamic and cingulate cortex lesions on object-in-place memory in monkeys

Six Macaque monkeys (Macaca mulatta) were trained in an object-in-place memory task, designed to capture the 'whole scene' nature of episodic memory. In this task the correct, rewarded, response in each scene was to a particular object of a pair, which always occupied a particular position in a unique background which had been generated using randomly chosen colours and shapes. In each session, the monkey learned a new list of these unique scenes. The animals then underwent surgical ablation of either the anterior thalamic nuclei or the cingulate cortex. It was found that the animals with anterior thalamic lesions showed a substantial impairment, whereas the monkeys with cingulate cortex ablations were not significantly impaired at the task. These results confirm the importance of the anterior thalamic nuclei in episodic memory, and suggest that the cingulate gyrus is not a region which is crucial in the type of episodic memory task used in the present experiment.

[1]  J. Aggleton,et al.  Both fornix and anterior thalamic, but not mammillary, lesions disrupt delayed non-matching-to-position memory in rats , 1991, Behavioural Brain Research.

[2]  I. Daum,et al.  Frontal-type memory impairment associated with thalamic damage. , 1994, The International journal of neuroscience.

[3]  M. Gabriel,et al.  Anterior thalamic lesions and neuronal activity in the cingulate and retrosplenial cortices during discriminative avoidance behavior in rabbits. , 1983, Behavioral neuroscience.

[4]  E. Murray,et al.  Preserved Recognition Memory for Small Sets, and Impaired Stimulus Identification for Large Sets, Following Rhinal Cortex Ablations in Monkeys , 1994, The European journal of neuroscience.

[5]  M. Kopelman.  The Korsakoff Syndrome , 1995, British Journal of Psychiatry.

[6]  R. Sutherland,et al.  Contributions of cingulate cortex to two forms of spatial learning and memory , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  Memory systems in primates: episodic, semantic, and perceptual learning , 1998 .

[8]  J. Aggleton,et al.  The effects of selective lesions within the anterior thalamic nuclei on spatial memory in the rat , 1996, Behavioural Brain Research.

[9]  G. Hankey,et al.  Amnesia following thalamic hemorrhage. Another stroke syndrome. , 1988, Stroke.

[10]  R. Passingham,et al.  The nucleus accumbens in monkeys (Macaca fascicularis): I. The organization of behaviour , 1994, Behavioural Brain Research.

[11]  R. Nitsch,et al.  Substance P-containing hypothalamic afferents to the monkey hippocampus: an immunocytochemical, tracing, and coexistence study , 1994, Experimental Brain Research.

[12]  J. Aggleton,et al.  Lack of effect of lesions in the anterior cingulate cortex and retrosplenial cortex on certain tests of spatial memory in the rat , 1994, Behavioural Brain Research.

[13]  M. Mishkin,et al.  Visual recognition impairment following medial thalamic lesions in monkeys , 1983, Neuropsychologia.

[14]  J. Aggleton,et al.  A comparison of the effects of medial prefrontal, cingulate cortex, and cingulum bundle lesions on tests of spatial memory: evidence of a double dissociation between frontal and cingulum bundle contributions , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  J. Aggleton,et al.  The contribution of the anterior thalamic nuclei to anterograde amnesia , 1993, Neuropsychologia.

[16]  G. W. Snedecor.  Statistical Methods , 1964 .

[17]  M. Gabriel,et al.  Discriminative Avoidance Learning: A Model System , 1993 .

[18]  R. Saunders,et al.  Running Recognition of Configural Stimuli by Fornix-Transected Monkeys , 1985, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[19]  J. W. Papez.  A PROPOSED MECHANISM OF EMOTION , 1937 .

[20]  P. Goldman-Rakic,et al.  The primate mediodorsal (MD) nucleus and its projection to the frontal lobe , 1985, The Journal of comparative neurology.

[21]  D. Pandya,et al.  Some observations on the course and composition of the cingulum bundle in the rhesus monkey , 1984, The Journal of comparative neurology.

[22]  D. Gaffan,et al.  Interaction of Perirhinal Cortex with the Fornix–Fimbria: Memory for Objects and “Object-in-Place” Memory , 1996, The Journal of Neuroscience.

[23]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[24]  M. Gabriel,et al.  Neurobiology of Cingulate Cortex and Limbic Thalamus , 1993 .

[25]  J. Aggleton,et al.  A comparison of the effects of anterior thalamic, mamillary body and fornix lesions on reinforced spatial alternation , 1995, Behavioural Brain Research.

[26]  K. Kultas‐Ilinsky,et al.  Sagittal cytoarchitectonic maps of the Macaca mulatta thalamus with a revised nomenclature of the motor‐related nuclei validated by observations on their connectivity , 1987, The Journal of comparative neurology.

[27]  M. Mishkin,et al.  A selective mnemonic role for the hippocampus in monkeys: memory for the location of objects , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  D. Gaffan.  Scene-Specific Memory for Objects: A Model of Episodic Memory Impairment in Monkeys with Fornix Transection , 1994, Journal of Cognitive Neuroscience.

[29]  G. J. Thomas,et al.  Mammillothalamic tracts and representational memory. , 1985, Behavioral neuroscience.

[30]  B. Vogt,et al.  Anterior Cingulate Cortex and the Medial Pain System , 1993 .

[31]  Elisabeth A. Murray,et al.  What have ablation studies told us about the neural substrates of stimulus memory , 1996 .

[32]  Amanda Parker,et al.  Mamillary Body Lesions in Monkeys Impair Object-in-Place Memory: Functional Unity of the Fornix-Mamillary System , 1997, Journal of Cognitive Neuroscience.

[33]  Jean Delay,et al.  Le Syndrome de Korsakoff , 1969 .