Integration of what and where in the primate prefrontal cortex

Science

Volumn 276, Issue 5313, 1997, Pages 821-824

  Rao, S Chenchal ^a   Rainer, Gregor ^a   Miller, Earl K ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; BEHAVIOR; COGNITION; LEARNING; MONKEY; NERVE CELL; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; SPATIAL MEMORY;

ANIMALS; BRAIN MAPPING; CUES; FIXATION, OCULAR; FORM PERCEPTION; MACACA FASCICULARIS; MACACA MULATTA; MEMORY; NEURONAL PLASTICITY; NEURONS; PREFRONTAL CORTEX; SACCADES; SPACE PERCEPTION; VISUAL PATHWAYS;

ANIMALIA; PRIMATES;

EID: 0030953250     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.276.5313.821     Document Type: Article

References (31)

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16. Eye position was monitored by means of the scleral search coil method [D. A. Robinson, IEEE Trans. Biomed. Eng. 10, 137 (1963)]. The sample and test objects were presented for 400 ms, and the delays were 1000 ms. The monkeys (Macaca fasicularis and Macaca mulatta) were required to maintain fixation of a central spot throughout the trial. At the end of the where delay, the fixation spot was extinguished and small (0.3°) spots appeared simultaneously at each of the four locations used in this task (Fig 1). This was the monkey's "go" signal. It then had to make a direct saccade to the spot that was at the location where the match had appeared. The four locations were on the horizontal and vertical meridians, 4° above, below, to the right, and to the left of fixation. The four objects were color pictures of "real world" objects 2° by 2° in size. Each object was used as a sample or match on some trials and as a non-match on other trials, and each object was used to cue each location. With this design, what and where are linked within a single trial, but across trials they are varied independently (that is, no object is exclusively linked with a location). The same four objects and locations were used throughout the experiment.
17. Recording sites were localized by magnetic resonance imaging.
18. Delay activity was analyzed over the last 800 ms of a 1000-ms delay. We did not include the first portion of the delay, to exclude any responses related to the offset of the preceding stimulus. On average, data from about 600 correctly performed trials (about 85% of the total trials) were collected from each cell.
19. We did not distinguish between location-tuned activity related to retaining sensory information about a location and activity related to a "motor set" of the forthcoming saccade. However, previous studies have found that the activity of most of the PF delay neurons is related to retaining sensory rather than motor information [S. Funahashi, M. V. Chafee, P. S. Goldman-Rakic, Nature 365, 753 (1993); G. DiPellegrino and S. P. Wise, J. Neurosci. 13, 1227 (1993)].
20. We did not distinguish between location-tuned activity related to retaining sensory information about a location and activity related to a "motor set" of the forthcoming saccade. However, previous studies have found that the activity of most of the PF delay neurons is related to retaining sensory rather than motor information [S. Funahashi, M. V. Chafee, P. S. Goldman-Rakic, Nature 365, 753 (1993); G. DiPellegrino and S. P. Wise, J. Neurosci. 13, 1227 (1993)].
21. We mapped a 12 mm by 12 mm extent of the lateral PF cortex at 1-mm intervals using a grid system (Crist Instruments, Damascus, MD). The recording chamber was centered on the principal sulcus. Its posterior end was 2 mm behind the bow of the arcuate sulcus. The dorsal and ventral recordings extended to about just above and below the superior and inferior arcuate sulci, respectively. The dorsolateral PF cortex lies in and dorsal to the principal sulcus, and the ventrolateral PF cortex lies on the inferior convexity, ventral to the principal sulcus. What cells, where cells, and what-and-where cells were found about equally in the dorsolateral and ventrolateral PF cortex. In the dorsolateral PF cortex, 3 what cells, 25 where cells, and 34 what-and-where cells were found. In the ventrolateral PF cortex 5 what cells, 26 where cells, and 30 what-and-where cells were found. The ANOVAs identified highly selective neurons; across the population, selectivity for what and for where varied along a continuum from nonselective neurons to highly selective neurons.
22. To eliminate any optimistic bias in the classification, we performed the discriminant analysis with cross-validation; that is, the distribution of means for each class was computed on half the data, chosen randomly, and these means were used to classify the objects or locations in the other half of the data.
23. Because the activity of individual neurons is "noisy," they rarely perform as well as the animal as a whole. By pooling the activity of multiple neurons, it is possible to reduce noise, and a neural classification rate equal to behavioral performance can thus be achieved [for details, see E. K. Miller, L. Li, R. Desimone, J. Neurosci. 13, 1460 (1993)].
24. Their relatively low classification rate for objects on the basis of where delay activity (28.3%) was not due to the generally poor ability of these neurons at classifying objects; their mean classification rate for objects on the basis of what delay activity was significantly greater (32.3%, P < 0.001). The lower rate could have been due, in principle, to an effect of the nonmatching object, which was not included in the classification and thus could add "noise." However, the mean classification rate of a discriminant analysis of the where delay activity that attempted to classify the nonmatching stimulus (24.8%) was not different from chance (P = 0.680), indicating no effect of the nonmatch on the where delay activity. Thus, the effect of object on the where delay activity appears to be due to the match object alone.
25. See J. M. Fuster, Memory in the Cerebral Cortex (MIT Press, Cambridge, MA, 1995).
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29. A neural network model also suggests that the extent to which what and where are segregated or integrated in the pretrontal cortex depends on task demands [T. S. Braver and J. D. Cohen, Proc. Cognit. Neurosci. Soc. 2, 95 (1995)].
30. G. H. Recanzone, M. M. Merzenich, W. M. Jenkins, A. G. Kamil, H. R. Dinse, J. Neurophysiol. 67, 1057 (1992).
31. Animal experiments were conducted in accordance with the MIT Committee on Animal Care. This work was supported by the Pew Charitable Trusts and the McKnight Foundation. We thank M. Histed for help in animal training and W. Asaad, R. Desimone, Y. Munakata, J. Mazer, R. O'Reilly, and M. Wicherski for valuable comments. S.C.R. was supported by a fellowship from the McDonnell-Pew Foundation and the Markey Foundation.