Brain Research, 544 (1991) 269-278
© 1991 Elsevier Science Publishers B.V. (Biomedical Division) 0006-8993/91/$03.50
ADONIS 000689939116443S
BRES 16443
269
Unit activity in the hippocampus and the parahippocampal
temporobasal association cortex related to memory and complex
behaviour in the awake monkey
T.R. Vidyasagar, E. Salzmann and O.D. Creutzfeldt
Department of Neurobiology, Max Planck Institutefor Biophysical Chemistry, G6ttingen (Germany)
(Accepted 16 October 1990)
Key words: Hippocampus; Parahippocampus; Memory; Awake monkey; Delayed match-to-sample task
Monkeys (Macacafascicularis) 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 dosed, 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.
INTRODUCTION
Bilateral damage in the monkey to the medial tempo-
ral lobe that includes the hippocampal formation, amyg-
dala and the adjacent inferomedial temporal cortex
produces profound alterations in behaviour, including
inappropriate responses to visual stimuli 22'24. In a human
patient with similar damage, an almost complete ante-
rograde amnesia extending to all sensory modalities has
been reported 8,4°. However, investigations of monkeys
with specific surgically placed lesions and human amne-
sics have not quite resolved the relative importance of the
different structures in the temporal lobe for the memory
deficit 11'19'21'27'29'30'42"50. Single-unit studies have also led
to somewhat conflicting results. Whereas some studies
have reported that neurones in the inferotemporal cortex
are active during the retention phase of a delayed
match-to-sample (DMS) task 14'31, other studies 4,6 have
found inferotemporal neurones that responded differen-
tially to the first and the second presentations of a
stimulus in a DMS task, but rarely found any that showed
increased activity in the delay period during which a
visual scene was being actively kept in memory. Record-
ings from human and monkey hippocampus 5,1°,16,1s,49
have shown various types of activity changes during
memory tasks, but only occasional responses during the
retention phase of a specific memory task. The hippo-
campus has also been implicated in a number of other
functions, such as spatial map 34, control of attention 12,23,
temporary associative memory2S,35, prevention of
interference 4s, working memory 3,36, discrimination of
familiarity vs novelty 15 and object-place association as.
Hippocampus has also a central place in the Papez
circuit 37 that attempted to provide a neural basis for
emotional behaviour (for review, see refs. 9 and 25).
The neocortical input reaching the hippocampus
through the perforant pathway is largely routed through
the entorhinal area, which in turn receives a massive
input from the parahippocampal temporo-basal cortex.
The temporo-basal cortex can be subdivided into several
regions based upon cytoarchitecture and connectivity 1.
One major subdivision is characterised by its bidirec-
tional connections with large parts of the parietal,
temporal and frontal association cortices 44,45,46, as well as
Correspondence: T.R. Vidyasagar. Present address: Division of Neuroscience, John Curtin School of Medical Research, Australian National
University, G.P.O. Box 334, Canberra, A.C.T. 2601, Australia.