Functional analysis of spatially discriminative neurons in prefrontal cortex of rhesus monkey

The present study addresses the question of whether prefrontal neurons that exhibit spatially selective patterns of discharge during the delay period in spatial delayed-response tasks code a mnemonic event. To examine this question, rhesus monkeys were trained to perform two variants of the classical spatial delayed-response task in both of which a delay intervened between cue presentation and response and the discriminative stimulus had to be recalled at the moment of response. They were also trained to perform two control tasks in which memory was not required since cues present throughout the delay informed the monkey of the correct response. Extracellular recordings were obtained from 192 neurons located in and around the principal sulcus of the frontal lobe during performance of both control and delay tasks. Comparison of the same neuron's activity across the 4 task conditions revealed a class of neuron that displayed spatially discriminative activity in the delay period only during delayed-response tasks and not during the same period of the control tasks. These neurons are candidates for units engaged in a central mnemonic process. Other neurons either exhibited similar activity in the delay period of control and delayed-response tasks or stronger discriminative behavior during this period in control tasks than in delayed response tasks. We conclude that delay-related spatially discriminative neurons found in the prefrontal association cortex are diversified and that certain of them play a specific role in mnemonic coding.

[1]  H. E. Rosvold,et al.  Analysis of the delayed-alternation deficit produced by dorsolateral prefrontal lesions in the rhesus monkey. , 1971, Journal of comparative and physiological psychology.

[2]  G. E. Alexander,et al.  Neuron Activity Related to Short-Term Memory , 1971, Science.

[3]  H. E. Rosvold,et al.  Localization of function within the dorsolateral prefrontal cortex of the rhesus monkey. , 1970, Experimental neurology.

[4]  J. Fuster Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. , 1973, Journal of neurophysiology.

[5]  A. Mikami,et al.  Visual response properties of dorsolateral prefrontal neurons during visual fixation task. , 1982, Journal of neurophysiology.

[6]  Shozo Kojima,et al.  Prefrontal neuron activity during delayed-response performance without imperative GO signals in the monkey , 1981, Experimental Neurology.

[7]  Analysis of changes in indirect delayed response performance in monkeys with prefrontal lesions. , 1969, Journal of comparative and physiological psychology.

[8]  S. Ito Prefrontal unit activity of macaque monkeys during auditory and visual reaction time tasks , 1982, Brain Research.

[9]  H Niki,et al.  Prefrontal unit activity during delayed alternation in the monkey. I. Relation to direction of response. , 1974, Brain research.

[10]  H. Komatsu,et al.  Prefrontal unit activity during a color discrimination task with GO and NO-GO responses in the monkey , 1982, Brain Research.

[11]  M. Sakai,et al.  Prefrontal unit activity during visually guided lever pressing reaction in the monkey. , 1974, Brain research.

[12]  P. Black,et al.  Delayed response capability after prefrontal ablation: a comparison of tasks and task circumstance. , 1976, The International journal of neuroscience.

[13]  Masataka Watanabe,et al.  Prefrontal unit activity and delayed response: Relation to cue location versus direction of response , 1976, Brain Research.

[14]  S. Kojima Prefrontal unit activity in the monkey: Relation to visual stimuli and movements , 1980, Experimental Neurology.

[15]  K. Kubota,et al.  Visuokinetic activities of primate prefrontal neurons during delayed-response performance. , 1974, Journal of neurophysiology.

[16]  H. Niki Differential activity of prefrontal units during right and left delayed response trials. , 1974, Brain research.

[17]  J. Fuster,et al.  Delayed-matching and delayed-response deficit from cooling dorsolateral prefrontal cortex in monkeys. , 1976, Journal of comparative and physiological psychology.

[18]  P. Goldman-Rakic,et al.  Operant behavioral analysis of memory loss in monkeys with prefrontal lesions , 1982, Brain Research.

[19]  M. Azuma,et al.  Prefrontal neuronal activity during gazing at a light spot in the monkey , 1977, Brain Research.

[20]  H. Harlow,et al.  A survey of delayed response performance by normal and brain damaged monkeys. , 1951, Journal of comparative and physiological psychology.

[21]  H Suzuki,et al.  Stimulus and behavioral factors contributing to the activation of monkey prefrontal neurons during gazing. , 1979, The Japanese journal of physiology.

[22]  H Niki,et al.  Prefrontal unit activity during delayed alternation in the monkey. II. Relation to absolute versus relative direction of response. , 1974, Brain research.

[23]  S. Kojima Short-term memory in the rhesus monkey: A behavioral analysis of delayed-response performance. , 1980, Journal of the experimental analysis of behavior.

[24]  H. Niki,et al.  Prefrontal cortical unit activity and delayed alternation performance in monkeys. , 1971, Journal of neurophysiology.

[25]  P. Goldman-Rakic,et al.  Delay-related activity of prefrontal neurons in rhesus monkeys performing delayed response , 1982, Brain Research.