The dorsolateral prefrontal cortex (PFC) has been implicated in visuospatial memory, and its cellular basis has been extensively studied with the delayed-response paradigm in monkeys. However, using this paradigm, it is difficult to dissociate neuronal activities related to visuospatial memory from those related to motor preparation, and few studies have provided evidence for the involvement of PFC neurons in visuospatial memory of a sensory cue, rather than in motor preparation. To extend this finding, we examined neuronal activities in the dorsolateral PFC while a rhesus monkey performed a spatial delayed matching-to-sample (SDMTS) task, which allows us to adequately access visuospatial memory independent of any sensorimotor components. The SDMTS task required the subject to make a lever-holding NOGO response or a lever-releasing GO response when a visuospatial matching cue (white spot, one of four peripheral locations, 15 degrees in eccentricity) matched or did not match a sample cue (physically the same as the matching cue) that had been presented prior to a delay period (3 s). Thus, the SDMTS task requires the subject to remember visuospatial information regarding the sample cue location during the delay period and is suitable for accessing visuospatial memory independent of any sensorimotor components, such as motor preparation, for directed movements. Of a total of 385 task-related neurons, 184 showed a sustained increase in activity during the delay period ("delay-period activity"). Most of these neurons (n = 165/184, 90%) showed positional delay-period activity, i.e., delay-period activity where the magnitude differed significantly with the position of the sample cue. This activity appears to be involved in visuospatial memory and to form a "memory field." To quantitatively examine the properties of positional delay-period activity, we introduced a tuning index (TI) and a discriminative index (DI), which represent the sharpness of tuning and the discriminative ability, respectively, of positional delay-period activity. Both TI and DI varied among neurons with positional delay-period activity and were closely related to the time from the onset of the sample cue to the onset of positional delay-period activity; positional delay-period activity with sharper tuning and a greater discriminative ability had a slower onset. Furthermore, at the population level, both TI and DI were increased during the delay period in the neuronal population with a high DI value. These results extend previous findings to suggest that integrative, convergent processes of neuronal activities for increasing the accuracy of visuospatial memory may occur in the dorsolateral PFC. Thus, a critical role of the dorsolateral PFC in visuospatial memory may be to sharpen it to guide behaviors/decisions requiring accurate visuospatial memory.
Abstract:The Japanese macaque (Macaca fuscata), along with rhesus and long-tailed macaques, is one of the macaca species. In Japan, it has been preferred for use as a laboratory animal, particularly in the field of neuroscience, because of its high level of intelligence and its gentle nature. In addition, the species has a relatively homogeneous genetic background and field researchers have accumulated abundant information on the social behavior of wild Japanese macaques. As future neuroscience research will undoubtedly be more focused on the higher cognitive functions of the brain, including social behavior among multiple individuals, the Japanese macaque can be expected to become even more valuable as a laboratory animal in the near future. The Ministry of Education, Culture, Sports, Science and Technology has launched a National BioResource Project (NBRP) to establish a stable breeding and supply system for Japanese macaques for laboratory use. The project is in progress and should lead to the establishment of a National Primate Center in Japan, which will support the supply of monkeys as well as social outreach and handling of animal welfare issues.
1. A gamma-aminobutyric acid (GABA) antagonist, bicuculline methiodide (BMI, 10 micrograms/microliters, 1 microliter), was locally injected into a total of 32 sites in the right premotor cortex (PM) of two rhesus monkeys that had been well-trained in a visually guided reaching task (VR) for approximately 3 yr. The monkey initiated the task by pressing a central hold lever with its left hand, and this was followed by waiting (1 s), warning (central green square on a computer monitor, 0.5 s), cue (right, upper, or left square), delay (2-5 s), and go (central green square changes to red, < 1.2 s) periods. In the go period, the monkey released the hold lever and reached out to one of three target levers (left, upper, or right) that had been indicated 2-5 s previously in the cue period. 2. At three sites in the dorsal part of the PM, after the local application of BMI, reaching movements of the left forelimb, which were not part of the trained-reaching, occurred 200-300 ms after the onset of a burst of neuronal activity at the BMI injection site. This induced-reaching, which was designated a "forced-reaching" movement, occurred while the monkeys were pressing the hold lever before the cue appeared-i.e., during the waiting or waiting period. No reaching occurred when the burst did not appear. Furthermore, trajectories and electromyograms of the forelimbs during the forced-reaching movements were similar to those in the trained-reaching movements in the VR task. 3. These results suggest that restricted sites in the dorsal PM of monkeys are involved in the initiation and/or execution of trained-reaching movements and that GABAergic inhibition at these sites normally suppresses this initiation/execution unless it is required. By relaxing GABAergic suppression, the dorsal PM might send a command to a neuronal system that is associated with trained reaching to recruit the system, thereby initiating and/or executing the trained reaching.
No abstract
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