Unit activity in the hippocampus and the parahippocampal temporobasal association cortex related to memory and complex behaviour in the awake monkey

Monkeys (Macaca fascicularis) were trained on a delayed match-to-sample (DMS) task using delays of upto 20 s. Unit activity was recorded from the hippocampus and the temporo-basal association cortex in the lateral parahippocampal region (partly corresponding to TF and TH) during the DMS task, as well as during a visual object discrimination task and some behavioural situations involving the experimenter. Units were encountered that gave visual responses which were sometimes context-dependent. Changes in discharge rate during the delay period of the DMS task were very rare and when present, very weak. On the other hand, many neurones, including some of those which were unresponsive during the DMS task fired vigorously (or were inhibited) during situations which involved attention, expectation or food consumption. For example, the neurones' firing rate was altered when the cage door was opened or closed, the experimenter entered or left the room or showed the monkey a piece of food before giving it to him. A variety of such responses in complex behavioural situations were seen, sometimes even in neurones which did not respond in the DMS task. Activity changes in neurons of the temporo-basal cortex thus appear to be related to the internal state associated with a stimulus and even some of the responses obtained in the DMS task can be interpreted as being related to changes in the behavioural state rather than to the mnemonic elements of the task.

[1]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[2]  Deepak N. Pandya,et al.  Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. II. Frontal lobe afferents , 1975, Brain Research.

[3]  A. Baddeley The concept of working memory: A view of its current state and probable future development , 1981, Cognition.

[4]  M. Mishkin A memory system in the monkey. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[5]  H M PERR,et al.  Criteria distinguishing parents of schizophrenic and normal children; an initial study with the interpersonal diagnostic system. , 1958, A.M.A. archives of neurology and psychiatry.

[6]  J M Fuster,et al.  Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  M. W. Brown,et al.  Neuronal evidence that inferomedial temporal cortex is more important than hippocampus in certain processes underlying recognition memory , 1987, Brain Research.

[8]  B. C. Motter,et al.  The functional properties of the light-sensitive neurons of the posterior parietal cortex studied in waking monkeys: foveal sparing and opponent vector organization , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  L. Squire Memory and Brain , 1987 .

[10]  S. Corkin Lasting Consequences of Bilateral Medial Temporal Lobectomy: Clinical Course and Experimental Findings in H.M. , 1984 .

[11]  Attention and eye movement related activation of neurons in the dorsal prelunate gyrus (area DP) , 1989, Brain Research.

[12]  James L Olds The central nervous system and the reinforcement of behavior. , 1969, The American psychologist.

[13]  Y. Miyashita,et al.  Hippocampal neurons in the monkey with activity related to the place in which a stimulus is shown , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  S. Iversen CHAPTER 5 – BRAIN LESIONS AND MEMORY IN ANIMALS: A REAPPRAISAL , 1983 .

[15]  L. Weiskrantz Comparative aspects of studies of amnesia. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[16]  G. Handelmann,et al.  Hippocampus, space, and memory , 1979 .

[17]  L. Squire,et al.  Human amnesia and animal models of amnesia: performance of amnesic patients on tests designed for the monkey. , 1988, Behavioral neuroscience.

[18]  D. Gaffan,et al.  Recognition impaired and association intact in the memory of monkeys after transection of the fornix. , 1974, Journal of comparative and physiological psychology.

[19]  J. O'Keefe,et al.  The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. , 1971, Brain research.

[20]  T L Babb,et al.  Activity of human hippocampal formation and amygdala neurons during memory testing. , 1978, Electroencephalography and clinical neurophysiology.

[21]  Dr. Juhani Hyvärinen The Parietal Cortex of Monkey and Man , 1982, Studies of Brain Function.

[22]  Y. Miyashita,et al.  Neuronal correlate of pictorial short-term memory in the primate temporal cortexYasushi Miyashita , 1988, Nature.

[23]  B. Fischer,et al.  Peripheral attention versus central fixation: Modulation of the visual activity of prelunate cortical cells of the rhesus monkey , 1985, Brain Research.

[24]  H. Klüver,et al.  PRELIMINARY ANALYSIS OF FUNCTIONS OF THE TEMPORAL LOBES IN MONKEYS , 1939 .

[25]  K. Pribram,et al.  Distraction and habituation in monkeys with limbic lesions. , 1969, Journal of comparative and physiological psychology.

[26]  M. Mishkin Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus , 1978, Nature.

[27]  Deepak N. Pandya,et al.  Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections , 1975, Brain Research.

[28]  H. Markowitsch Can Amnesia be Caused by Damage of a Single Brain Structure? , 1984, Cortex.

[29]  M. Mishkin,et al.  Limbic lesions and the problem of stimulus--reinforcement associations. , 1972, Experimental neurology.

[30]  J. A. Horel The neuroanatomy of amnesia. A critique of the hippocampal memory hypothesis. , 1978, Brain : a journal of neurology.

[31]  E. Warrington,et al.  New Method of Testing Long-term Retention with Special Reference to Amnesic Patients , 1968, Nature.

[32]  D. Bouis,et al.  An accurate and linear infrared oculometer , 1983, Journal of Neuroscience Methods.

[33]  G. V. Hoesen,et al.  The parahippocampal gyrus: New observations regarding its cortical connections in the monkey , 1982, Trends in Neurosciences.

[34]  H. Niki,et al.  Hippocampal unit activity and delayed response in the monkey , 1985, Brain Research.

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

[36]  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.

[37]  E. Halgren,et al.  Neural encoding of individual words and faces by the human hippocampus and amygdala , 1988, Nature.

[38]  P. Dean Effects of inferotemporal lesions on the behavior of monkeys. , 1976, Psychological bulletin.

[39]  E. Rolls,et al.  Activity of hippocampal formation neurons in the monkey related to a conditional spatial response task. , 1989, Journal of neurophysiology.

[40]  E. T. Rolls,et al.  Responses of hippocampal formation neurons in the monkey related to delayed spatial response and object-place memory tasks , 1989, Behavioural Brain Research.

[41]  D. Kimble Hippocampus and internal inhibition. , 1968, Psychological bulletin.