Crossed unilateral lesions of medial forebrain bundle and either inferior temporal or frontal cortex impair object recognition memory in Rhesus monkeys

In monkeys, section of the fornix, amygdala and anterior temporal stem results in a severe anterograde amnesia. Immunolesions of the cholinergic cells of the basal forebrain suggest that this amnesia is a result of isolating the inferior temporal cortex and medial temporal lobe from their cholinergic basal forebrain afferents. In this experiment, six monkeys were trained in a delayed match-to-sample task and then received a section of the medial forebrain bundle in one hemisphere and an ablation of either the frontal or inferior temporal cortex in the opposite hemisphere. All the animals were severely impaired in the performance of this task following this surgery, and the severity of the impairment was independent of the cortical area from which the medial forebrain bundle was disconnected. These results support a model of fronto-temporal interaction via the basal forebrain in new learning, in which midbrain sites related to reward modulate the cholinergic basal forebrain activity.

[1]  D. Gaffan,et al.  Single and Concurrent Discrimination Learning by Monkeys after Lesions of Inferotemporal Cortex , 1986, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[2]  M. Delong,et al.  Fiber pathways of basal forebrain cholinergic neurons in monkeys , 1987, Brain Research.

[3]  M. J. Eacott,et al.  Inferotemporal‐frontal Disconnection: The Uncinate Fascicle and Visual Associative Learning in Monkeys , 1992, The European journal of neuroscience.

[4]  S. Gutnikov,et al.  Monkeys can associate visual stimuli with reward delayed by 1 s even after perirhinal cortex ablation, uncinate fascicle section or amygdalectomy , 1997, Behavioural Brain Research.

[5]  J. A. Horel,et al.  Lesions of the anterior temporal stem and the performance of delayed match-to-sample and visual discriminations in monkeys , 1989, Behavioural Brain Research.

[6]  M. Mesulam,et al.  Trajectories of cholinergic pathways within the cerebral hemispheres of the human brain. , 1998, Brain : a journal of neurology.

[7]  J. Hollerman,et al.  Dopamine neurons report an error in the temporal prediction of reward during learning , 1998, Nature Neuroscience.

[8]  L. Záborszky,et al.  Catecholaminergic-cholinergic interaction in the basal forebrain. , 1993, Progress in brain research.

[9]  M. Mishkin.  Visual discrimination performance following partial ablations of the temporal lobe. II. Ventral surface vs. hippocampus. , 1954, Journal of comparative and physiological psychology.

[10]  M. Voytko.  Cooling orbital frontal cortex disrupts matching-to-sample and visual discrimination learning in monkeys , 1985 .

[11]  John Patrick Aggleton,et al.  The Amygdala : a functional analysis , 2000 .

[12]  D. Gaffan,et al.  Dense amnesia in the monkey after transection of fornix, amygdala and anterior temporal stem , 2001, Neuropsychologia.

[13]  E. Miller,et al.  The prefontral cortex and cognitive control , 2000, Nature Reviews Neuroscience.

[14]  A. Cuello,et al.  Afferents to the basal forebrain cholinergic cell area from pontomesencephalic—catecholamine, serotonin, and acetylcholine—neurons , 1989, Neuroscience.

[15]  D. Gaffan,et al.  Comparison of perirhinal cortex ablation and crossed unilateral lesions of the medial forebrain bundle from the inferior temporal cortex in the rhesus monkey: effects on learning and retrieval. , 2000, Behavioral neuroscience.

[16]  Rudolf Nieuwenhuys,et al.  Chemoarchitecture of the Brain , 1985, Springer Berlin Heidelberg.

[17]  C. J. Maclean,et al.  Learning impairments following injection of a selective cholinergic immunotoxin, ME20.4 IgG-saporin, into the basal nucleus of Meynert in monkeys , 1997, Neuroscience.

[18]  H. Barbas,et al.  Topographic Organization of Connections between the Hypothalamus and Prefrontal Cortex in the Rhesus Monkey , 2022 .

[19]  D. Gaffan,et al.  Crossed unilateral lesions of the medial forebrain bundle and either inferior temporal or frontal cortex impair object–reward association learning in Rhesus monkeys , 2001, Neuropsychologia.

[20]  David Gaffan,et al.  Visual Identification following Inferotemporal Ablation in the Monkey , 1986, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[21]  Amanda Parker,et al.  Memory after frontal/temporal disconnection in monkeys: conditional and non-conditional tasks, unilateral and bilateral frontal lesions , 1998, Neuropsychologia.

[22]  C. J. Maclean,et al.  Severe learning impairment caused by combined immunotoxic lesion of the cholinergic projections to the cortex and hippocampus in monkeys , 1999, Brain Research.

[23]  C. J. Maclean,et al.  Different effects on learning ability after injection of the cholinergic immunotoxin ME20.4IgG-saporin into the diagonal band of Broca, basal nucleus of Meynert, or both in monkeys. , 1999, Behavioral neuroscience.

[24]  L. Záborszky,et al.  Organization of ascending hypothalamic projections to the rostral forebrain with special reference to the innervation of cholinergic projection neurons , 1991, The Journal of comparative neurology.

[25]  K. Nakamura,et al.  Hypothalamic neuron involvement in integration of reward, aversion, and cue signals. , 1986, Journal of neurophysiology.

[26]  E. Rolls,et al.  The latency of activation of neurones in the lateral hypothalamus and substantia innominata during feeding in the monkey , 1979, Brain Research.

[27]  Mortimer Mishkin,et al.  Visual recognition impairment follows ventromedial but not dorsolateral prefrontal lesions in monkeys , 1986, Behavioural Brain Research.

[28]  D. Gaffan,et al.  Interaction of frontal and perirhinal cortices in visual object recognition memory in monkeys , 1998, The European journal of neuroscience.

[29]  E. T. Rolls,et al.  Activity of neurones in the inferotemporal cortex of the alert monkey , 1977, Brain Research.

[30]  J. A. Horel,et al.  The performance of visual tasks while segments of the inferotemporal cortex are suppressed by cold , 1987, Behavioural Brain Research.

[31]  W. Schultz,et al.  Responses of monkey dopamine neurons during learning of behavioral reactions. , 1992, Journal of neurophysiology.