Specialization and hierarchy are organizing principles for primate cortex, yet there is little direct evidence for how cortical areas are specialized in the temporal domain. We measured timescales of ...intrinsic fluctuations in spiking activity across areas and found a hierarchical ordering, with sensory and prefrontal areas exhibiting shorter and longer timescales, respectively. On the basis of our findings, we suggest that intrinsic timescales reflect areal specialization for task-relevant computations over multiple temporal ranges.
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Neurons in the middle temporal visual area (MT) have been implicated in the perception of visual motion, whereas prefrontal cortex (PFC) neurons have been linked to temporary storage of sensory ...signals, attentional and executive control of behavior. Using a task that placed demands on both sets of neurons, we investigated their contribution to working memory for visual motion. Monkeys compared the direction of two moving random-dot stimuli, sample and test, separated by a brief memory delay. Neurons in both areas showed robust direction-selective activity during all phases of the task. During the sample, approximately 60% of task-related PFC neurons were direction selective, and this selectivity emerged 40 ms later than in MT. Unlike MT, the PFC responses to sample did not correlate with behavioral choices, but their selectivity was modulated by task demands and diminished on error trials. Reliable directional signals were found in both areas during the memory delay, but these signals were transient rather than sustained by neurons of either area. Responses to the test in both areas were modulated by the remembered sample direction, decreasing when the test direction matched the sample. This decrease arose in the PFC 100 ms later than in MT and was predictive of the forthcoming decision. Our data suggest that neurons in the two regions are functionally connected and make unique contributions to different task components. PFC neurons reflect task-related information about visual motion and represent decisions that may be based, in part, on the comparison in MT between the remembered sample and test.
Neuronal activity in the lateral prefrontal cortex (LPFC) reflects the structure and cognitive demands of memory-guided sensory discrimination tasks. However, we still do not know how neuronal ...activity articulates in network states involved in perceiving, remembering, and comparing sensory information during such tasks. Oscillations in local field potentials (LFPs) provide fingerprints of such network dynamics. Here, we examined LFPs recorded from LPFC of macaques while they compared the directions or the speeds of two moving random-dot patterns, S1 and S2, separated by a delay. LFP activity in the theta, beta, and gamma bands tracked consecutive components of the task. In response to motion stimuli, LFP theta and gamma power increased, and beta power decreased, but showed only weak motion selectivity. In the delay, LFP beta power modulation anticipated the onset of S2 and encoded the task-relevant S1 feature, suggesting network dynamics associated with memory maintenance. After S2 onset the difference between the current stimulus S2 and the remembered S1 was strongly reflected in broadband LFP activity, with an early sensory-related component proportional to stimulus difference and a later choice-related component reflecting the behavioral decision buildup. Our results demonstrate that individual LFP bands reflect both sensory and cognitive processes engaged independently during different stages of the task. This activation pattern suggests that during elementary cognitive tasks, the prefrontal network transitions dynamically between states and that these transitions are characterized by the conjunction of LFP rhythms rather than by single LFP bands.
Neurons in the brain communicate through electrical impulses and coordinate this activity in ensembles that pulsate rhythmically, very much like musical instruments in an orchestra. These rhythms change with "brain state," from sleep to waking, but also signal with different oscillation frequencies rapid changes between sensory and cognitive processing. Here, we studied rhythmic electrical activity in the monkey prefrontal cortex, an area implicated in working memory, decision making, and executive control. Monkeys had to identify and remember a visual motion pattern and compare it to a second pattern. We found orderly transitions between rhythmic activity where the same frequency channels were active in all ongoing prefrontal computations. This supports prefrontal circuit dynamics that transitions rapidly between complex rhythmic patterns during structured cognitive tasks.
During motion discrimination tasks, many prefrontal cortex (PFC) neurons are strongly modulated by the behavioral context, suggesting their involvement in sensory discriminations. Recent studies ...suggest that trial-to-trial variability of spiking activity characteristic of cortical neurons could be a source of information about the state of neurons and their participation in behavioral tasks. We tested this hypothesis by examining the variability of putative pyramidal PFC neurons, a likely source of top-down influences. The variability of these neurons was calculated as a ratio of spike count variance to its mean (fano factor, FF), while monkeys compared the directions of two moving stimuli, sample and test, separated by a delay. We found that the FF tracked consecutive components of the task, dropping rapidly with the onset of stimuli being discriminated and declining more slowly before each salient event of the trial: The sample, the test, and the response. These time-dependent signals were less consistent in direction selective neurons and were largely absent during passive fixation. Furthermore, neurons with test responses that reflected the remembered sample decreased their FF well before the test, revealing the predictive nature of response variability, an effect present only during the active task. The FF was also sensitive to behavioral performance, exhibiting different temporal dynamics on error trials. These changes did not depend on firing rates and were often the only metric correlated with task demands. Our results demonstrate that trial-to-trial variability provides a sensitive measure of the engagement of putative pyramidal PFC neurons in circuits subserving discrimination tasks.
Comparing two stimuli that occur at different times demands the coordination of bottom-up and top-down processes. It has been hypothesized that the dorsolateral prefrontal (PFC) cortex, the likely ...source of top-down cortical influences, plays a key role in such tasks, contributing to both maintenance and sensory comparisons. We examined this hypothesis by recording from the PFC of monkeys comparing directions of two moving stimuli, S1 and S2, separated by a memory delay. We determined the contribution of the two principal cell types to these processes by classifying neurons into broad-spiking (BS) putative pyramidal cells and narrow-spiking (NS) putative local interneurons. During the delay, BS cells were more likely to exhibit anticipatory modulation and represent the remembered direction. While this representation was transient, appearing at different times in different neurons, it weakened when direction was not task relevant, suggesting its utility. During S2, both putative cell types showed comparison-related activity modulations. These modulations were of two types, each carried by different neurons, which either preferred trials with stimuli moving in the same direction or trials with stimuli of different directions. These comparison effects were strongly correlated with choice, suggesting their role in circuitry underlying decision making. These results provide the first demonstration of distinct contributions made by principal cell types to memory-guided perceptual decisions. During sensory stimulation both cell types represent behaviorally relevant stimulus features contributing to comparison and decision-related activity. However in the absence of sensory stimulation, putative pyramidal cells dominated, carrying information about the elapsed time and the preceding direction.
When a monkey needs to decide whether motion direction of one stimulus is the same or different as that of another held in working memory, neurons in dorsolateral prefrontal cortex (DLPFC) faithfully ...represent the motion directions being evaluated and contribute to their comparison. Here, we examined whether DLPFC neurons are more generally involved in other types of sensory comparisons. Such involvement would support the existence of generalized sensory comparison mechanisms within DLPFC, shedding light on top-down influences this region is likely to provide to the upstream sensory neurons during comparison tasks. We recorded activity of individual neurons in the DLPFC while monkeys performed a memory-guided decision task in which the important dimension was the speed of two sequentially presented moving random-dot stimuli. We found that many neurons, both narrow-spiking putative local interneurons and broad-spiking putative pyramidal output cells, were speed-selective, with tuning reminiscent of that observed in the motion processing middle temporal (MT) cortical area. Throughout the delay, broad-spiking neurons were more active, showing anticipatory rate modulation and transient periods of speed selectivity. During the comparison stimulus, responses of both cell types were modulated by the speed of the first stimulus, and their activity was highly predictive of the animals' behavioral report. These results are similar to those found for comparisons of motion direction, suggesting the existence of generalized neural mechanisms in the DLPFC subserving the comparison of sensory signals.
Department of Neurobiology and Anatomy and Center for Visual Science, University of Rochester, Rochester, New York 14642
Submitted 5 September 2003;
accepted in final form 27 September 2003
We ...recorded the activity of middle temporal (MT) neurons in 2 monkeys while they compared the directions of motion in 2 sequentially presented random-dot stimuli, sample and test, and reported them as the same or different by pressing one of 2 buttons. We found that MT neurons were active not only in response to the sample and test stimuli but also during the 1,500-ms delay separating them. Most neurons showed a characteristic pattern of activity consisting of a small burst of firing early in the delay, followed by a period of suppression and a subsequent increase in firing rate immediately preceding the presentation of the test stimulus. In a third of the neurons, the activity early in the delay not only reflected the direction of the sample stimulus, but was also related to the range of local directions it contained. During the middle of the delay the majority of neurons were suppressed, consistent with a gating mechanism that could be used to ignore task-irrelevant stimuli. Late in the delay, most neurons showed an increase in response, probably in anticipation of the upcoming test. Throughout most of the delay there was a directional signal in the population of MT neurons, manifested by higher firing rates following the sample moving in the antipreferred direction. Whereas some of these effects may be related to sensory adaptation, others are more likely to represent a more active task-related process. These results support the hypothesis that MT neurons actively participate in the successful execution of all aspects of the task requiring processing and remembering visual motion.
Address for reprint requests and other correspondence: T. Pasternak, Department of Neurobiology and Anatomy, Box 603, University of Rochester, Rochester, NY 14642 (E-mail: tania{at}cvs.rochester.edu ).
Psychophysical and neurophysiological studies of responses to visual motion have converged on a consistent set of general principles that characterize visual processing of motion information. Both ...types of approaches have shown that the direction and speed of target motion are among the most important encoded stimulus properties, revealing many parallels between psychophysical and physiological responses to motion. Motivated by these parallels, this review focuses largely on more direct links between the key feature of the neuronal response to motion, direction selectivity, and its utilization in memory-guided perceptual decisions. These links were established during neuronal recordings in monkeys performing direction discriminations, but also by examining perceptual effects of widespread elimination of cortical direction selectivity produced by motion deprivation during development. Other approaches, such as microstimulation and lesions, have documented the importance of direction-selective activity in the areas that are active during memory-guided direction comparisons, area MT and the prefrontal cortex, revealing their likely interactions during behavioral tasks.
Sensory working memory consists of the short-term storage of sensory stimuli to guide behaviour. There is increasing evidence that elemental sensory dimensions - such as object motion in the visual ...system or the frequency of a sound in the auditory system - are stored by segregated feature-selective systems that include not only the prefrontal and parietal cortex, but also areas of sensory cortex that carry out relatively early stages of processing. These circuits seem to have a dual function: precise sensory encoding and short-term storage of this information. New results provide insights into how activity in these circuits represents the remembered sensory stimuli.
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DOBA, IJS, IZUM, KILJ, NUK, PILJ, PNG, SAZU, UILJ, UKNU, UL, UM, UPUK
Working memory in primate sensory systems Pasternak, Tatiana; Greenlee, Mark W
Nature reviews. Neuroscience,
200503, 20050301, Letnik:
6, Številka:
3
Journal Article
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