topographic studies on visual neurons in the dorsolateral prefrontal cortex of the monkey

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  • Exp Brain Res (1983) 53:47-58 E . _mental Brain Research 9 Springer-Verlag 1983

    Topographic Studies on Visual Neurons in the Dorsolateral Prefrontal Cortex of the Monkey*

    H. Suzuki and M. Azuma

    Dept. of Physiology, Hirosaki University Faculty of Medicine, Hirosaki 036, Japan

    Summary. The topographic distribution and organi- zation of visual neurons in the prefrontal cortex was examined in alert monkeys. The animal was trained to fixate straight ahead onto a tinty, dim light spot. While he was fixating, we presented a stationary second light spot (RF spot) at various locations in the visual field and examined unit responses of the prefrontal neurons to the RF-spot stimulus. Many prefrontal neurons, especially those located in the relatively superficial layers of the cortex, responded with a phasic and/or tonic activation to the RF spot illuminating a limited extent of the visual field, a receptive field (RF) being so determined. The visual neurons were found to be widely distributed in the prearcuate and inferior dorsolateral areas. One hemisphere mainly represented the contralateral vis- ual field. According to the location of the neurons in these areas, their visual properties varied with re- spect to RF eccentricity from the fovea and in size. The neurons located in the lateral part of the areas and close to the inferior arcuate sulcus had relatively small RFs representing the foveal and parafoveal regions. When the recording site was moved medially, the RFs became eccentric from the fovea and were larger. Then, the neurons located between the caudal end of the principal sulcus and the arcuate sulcus had RFs with a considerable eccentricity. The size of the RF became progressively larger for anteriorly located neurons and this occurred gener- ally without a change in RF eccentricity. The visual neurons were not organized on a regular pattern in the cortex with regard to their RF direction (vector angle) from the foveal region. From these observa- tions, we conclude, first, that the prearcuate and inferior dorsolateral areas of the prefrontal cortex

    * Supported by Grant-in-aid for Scientific Research 444022, 587030 and Special Project Research Grant 56121-- [ from the Ministry of Education, Science and Culture of Japan

    Offprint requests to: Hisao Suzuki, MD (address see above)

    are functionally differentiated so that the lateral area's function is related to central vision, while that of the medial area to ambient vision. Second, the RF representation on the cortex with loss of the vector relation may generate an interaction between sepa- rate objects in visual space and may subserve the control of attention ]performance.

    Key words: Visual neuron - Prefrontal cortex - Alert monkey - Visual representation - Visual receptive field


    In a previous paper', we showed that the inferior dorsolateral and inferior prearcuate areas (IDL) of the prefrontal cortex contain many neurons which increase their discharge rate during foveal fixation on a light spot (Suzuki and Azuma 1977). Further investigation revealed that the activation includes several visual processes including an intentional one (Suzuki et al. 1979). These cortical regions may mediate functions concerned with central vision such as visual foveation to an object or visual attention in a broad sense. On the other hand, the prearcuate area posterior to the end of the principal sulcus seems to mediate processes relating to ambient vision. Using alert monkeys, Mohler et al. (1973) found neurons in the area that had a relatively large receptive field (RF) often located in the peripheral visual field contralateral to the recording hemi- sphere. The neurons did not show activation during fixation to a visual stimulus per se, indicating that they had rather peripheral RFs, sparing the fovea. These neurons frequently showed an enhancement of their visual response when the animal made a saccade to a stimulus in the RF (Wurtz and Mohler 1976;

  • 48 H. Suzuki and M. Azuma: Topography of Prefrontal Neurons

    Goldberg and Bushnell 1981). Such a functional differentiation within the prefrontal cortex in terms of neuronal location was also described by Pigarev et al. (1979). Neurons anteriorly located in the ar- cuate region required more complex visual stimuli for their activation as compared to posteriorly located neurons.

    Thus, it is expected that a wide area of the prefrontal cortex is concerned with the processing of visual information, and may further be differentiated with respect to specific visual functions. Recently, Mikami et al. (1982) found visual neurons over a wide area of prefrontal cortex, but they did not mention the areal differences of their neuronal properties. In this paper, we report the investigation of a neuron population widely located in the periprin- cipal and periarcuate areas of the prefrontal cortex in order to elucidate their different visual properties with particular reference to properties of visual RF. A preliminary report has appeared elsewhere (Azuma and Suzuki 1981).


    Training of Fixation Behavior

    Six male monkeys (Macaca rnulatta) weighing 5.0-8.4 kg were used. The monkeys were first trained to gaze steadily at a tiny, dim light spot (Wurtz 1969; Suzuki and Azuma 1977; Suzuki et al. 1979; Mikami et al. 1982). Each animal was seated in a primate chair facing a translucent screen 1.5 x 1.5 m square, illuminated diffusely at 1 cd/m 2 and placed 58 cm away from his eyes. After an intertrial interval of 4--6 s, a tiny, faint spot appeared on the center of the screen. By pressing a lever in front of him, the center spot stayed on for a duration of multiples of 0.5 s from 1 to 4 s, and then it slightly brightened for 0.5 s. A rapid lever-release within this bright period (except for the first 0.2 s) resulted in the delivery of 0.1-0.2 ml of orange-flavored sweet juice with the turning off of the light spot. The light spot was as small as 0.1 ~ in visual angle and the level of brightening was near-threshold for detection. There- fore, the monkey could not detect the brightening unless he gazed directly at the spot. Thus, a continuous gaze behavior was elicited during the light-spot presentation.

    The training method for this fixation task was described in detail in other papers (Suzuki and Azuma 1977; Suzuki et al. 1979). In this training for fixation, it was essential that very early in the training period the animal was taught to select the center spot as the only cue for getting the reward. Otherwise, various kinds of timing behavior were elicited which remained for long periods and led to long periods of training. It took 2 weeks - 1 month to establish the fixation behavior.


    After the above training was completed, a cylinder (20 mm diameter) for attaching a microelectrode positioner was implanted in the skull under Sernylan (phencyclidine hydrochloride) anes- thesia. Bolts and nuts specially designed for restraining the monkey's head were also anchored to .the skull. These implants

    were all made of Ni-Co-Mo alloy (Nippon Kinzoku, 22A) which was formed for orthopedic use to elicit negligible reactions by the animal's tissue.

    The experiments to examine the visual properties of prefron- tal neurons were started 2 weeks or more after the surgery when any damage of the brain due to surgery had been virtually recovered from. To control infection, Kanamycin sulfate (Banyu) was injected into the animal once a day.

    Presentation of Receptive Field Stimulus

    In the experimental sessions, the monkey was seated in a primate chair with his head immobilized by the implanted bolts, perform- ing the fixation task. During maintained fixation of the center spot, a second light (RF spot) was projected via a double galvanometer mirror system onto various parts of screen (90 x 90~ The second light was used to define the RF of neurons under study. It was usually a round spot, presented 0.5 s after a lever- press and lasting for 1 s. Its rise time was reduced to 5 ms by a feed-back circuit. Neutral density filters were used so that its intensity level was kept at 1.0-1.5 log units above background.

    While the center spot remained on, the monkey usually maintained fixation until the brightened, and made no eye movements toward the second spot. The eye position was moni- tored as horizontal and vertical electroculograms (EOGs). Inap- propriate eye movements occurring during the fixation period were detected by means of EOGs, and the trial was terminated automatically by an interposed 3 s time-out, a 5 ~ red-spot appear- ing in the center of the screen.

    Stimulus generation, sequential control of the manipulandum during the trials and the presentation of RF light were carried out by a programmable controller developed in our laboratory.

    Unit Recording and Data Processing

    For recording unit activity, a microelectrode positioner (Narishige, MO-9) was attached to the implanted cylinder. With this device we could insert a glass-insulated Elgiloy microelectrode (Suzuki and Azuma 1976, 1979) through the intact dura into a desired location of the prefrontal cortex. The electrode had a sharp tip which was exposed 15-25 Ixm from the electrode insulation. Care was taken to sterilize the electrode, instruments and wound area. Typically, one penetration of the microelectrode into the cortex was under- taketi dally with a series of penetrations made at 1 mm intervals.

    Unit activities were conventionally amplified and passed through a window discriminator. The converted pulses, together with EOGs and event signals, were fed into an interface led into a Nippon Data General 01 computer. Signals were processed on-line and shown on a computer display terminal (Tektronix, 4010-1) as raster patterns and peristimulus time histogram with respect to behavio


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