Prefrontal representation of stimulus attributes during delay tasks. I. Unit activity in cross-temporal integration of sensory and sensory-motor information

The activity of 294 single units was recorded from the dorsolateral prefrontal cortex of monkeys performing two visual discrimination tasks with delayed response. One task, delayed matching-to-sample (DMS), required memory of a colored cue for later (18 s) matching and choice of color; the cue did not connote the location of the delayed response. The other task, delayed conditional position discrimination (DCPD), required memory of a colored cue for later (18 s) choice of spatial response; the cue did connote delayed-response location. All 4 cues (red and green in DMS, yellow and blue in DCPD) were isoluminous and appeared in identical location at trial start. Differential unit reactions to the two DCPD cues were more common than those to the two DMS cues (samples). During the delay period, 15% of all units showed, in one task or the other, differential discharge depending on the cue. In DCPD, a large proportion of the units showing direction-related activity at the time of motor response also reacted with a firing frequency change to one or both (spatially identical) trial-initiating cues. Some units showed coherence of cue-related and response-related changes in accord with the behavioral association between color and direction of response (i.e., yellow-right, blue-left). The reactivity of some units was correlated with the behavioral performance of the tasks in terms of correctness or incorrectness of response. The results indicate that, during visual delay tasks, neurons in the dorsolateral prefrontal cortex may process both spatial and non-spatial information. Because of their protracted differential discharge between cue and response (i.e., during the delay), some units seem involved in the transfer of sensory information across time. These findings suggest the role of prefrontal neurons in the representation of multiple attributes of sensory stimuli, including their associated motor connotations, and the overlap of the cortical representations of different attributes. They are also consistent with the role of the prefrontal cortex in the cross-temporal mediation of sensory-motor contingencies and, therefore, the temporal organization of behavior.

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

[2]  Batuev As,et al.  Short-term spatiotemporal memory and cortical unit reactions in the monkey. , 1981 .

[3]  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.

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

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

[6]  J. Fuster,et al.  Prefrontal representation of stimulus attributes during delay tasks. II. The role of behavioral significance , 1988, Brain Research.

[7]  Shozo Kojima,et al.  Functional analysis of spatially discriminative neurons in prefrontal cortex of rhesus monkey , 1984, Brain Research.

[8]  J. Fuster,et al.  Cellular discharge in the dorsolateral prefrontal cortex of the monkey in cognitive tasks , 1982, Experimental Neurology.

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

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

[11]  H. W. Bond,et al.  Solid miniature silver-silver chloride electrodes for chronic implantation. , 1970, Electroencephalography and clinical neurophysiology.

[12]  Hisao Nishijo,et al.  Single neuron activity in dorsolateral prefrontal cortex of monkey during operant behavior sustained by food reward , 1984, Brain Research.

[13]  R E Passingham Memory of monkeys (Macaca mulatta) with lesions in prefrontal cortex. , 1985, Behavioral neuroscience.

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

[15]  J. Fuster The prefrontal cortex, mediator of cross-temporal contingencies. , 1985, Human neurobiology.

[16]  Masataka Watanabe,et al.  Cingulate unit activity and delayed response , 1976, Brain Research.

[17]  J M Fuster,et al.  Visual short-term memory deficit from hypothermia of frontal cortex. , 1974, Brain research.

[18]  C. Butter,et al.  Habituation of Responses to Novel Stimuli in Monkeys with Selective Frontal Lesions , 1964, Science.

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

[20]  Joaquin M. Fuster,et al.  Frontal cell activity during delayed response performance in squirrel monkey (Saimiri sciureus) , 1980, Physiology & Behavior.

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

[22]  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.