Directed Coupling in Local Field Potentials of Macaque V4 During Visual Short-Term Memory Revealed by Multivariate Autoregressive Models

Processing and storage of sensory information is based on the interaction between different neural populations rather than the isolated activity of single neurons. In order to characterize the dynamic interaction and transient cooperation of sub-circuits within a neural network, multivariate autoregressive (MVAR) models have proven to be an important analysis tool. In this study, we apply directed functional coupling based on MVAR models and describe the temporal and spatial changes of functional coupling between simultaneously recorded local field potentials in extrastriate area V4 during visual memory. Specifically, we compare the strength and directional relations of coupling based on generalized partial directed coherence (GPDC) measures while two rhesus monkeys perform a visual short-term memory task. In both monkeys we find increases in theta power during the memory period that are accompanied by changes in directed coupling. These interactions are most prominent in the low frequency range encompassing the theta band (3–12 Hz) and, more importantly, are asymmetric between pairs of recording sites. Furthermore, we find that the degree of interaction decreases as a function of distance between electrode positions, suggesting that these interactions are a predominantly local phenomenon. Taken together, our results show that directed coupling measures based on MVAR models are able to provide important insights into the spatial and temporal formation of local functionally coupled ensembles during visual memory in V4. Moreover, our findings suggest that visual memory is accompanied not only by a temporary increase of oscillatory activity in the theta band, but by a direction-dependent change in theta coupling, which ultimately represents a change in functional connectivity within the neural circuit

Color and shape interactions in the recognition of natural scenes by human and monkey observers

Trichromatic color vision is a fundamental aspect of the visual system shared by humans and non-human primates. In human observers, color has been shown to facilitate object identification. However, little is known about the role that color plays in higher level vision of non-human primates. Here, we addressed this question and studied the interaction between luminance- and color-based structural information for the recognition of natural scenes. We present psychophysical data showing that both monkey and human observers equally profited from color when recognizing natural scenes, and they were equally impaired when scenes were manipulated using colored noise. This effect was most prominent for degraded image conditions. By using a specific procedure for stimulus degradation, we found that the improvement as well as the impairment in visual memory performance is due to contribution of image color independent of luminance-based object information. Our results demonstrate that humans as well as non-human primates exploit their sensory ability of color vision to achieve higher performance in visual recognition tasks especially when shape features are degraded

Dissociable effects of natural image structure and color on LFP and spiking activity in the lateral prefrontal cortex and extrastriate visual area V4

Visual perception is mediated by unique contributions of the numerous brain regions that constitute the visual system. We performed simultaneous recordings of local field potentials (LFPs) and single unit activity (SUA) in areas V4 and lateral prefrontal cortex to characterize their contribution to visual processing. Here, we trained monkeys to identify natural images at different degradation levels in a visual recognition task. We parametrically varied color and structural information of natural images while the animals were performing the task. We show that the visual-evoked potential (VEP) of the LFP in V4 is highly sensitive to color, whereas the VEP in prefrontal cortex predominantly depends on image structure. When examining the relationship between VEP and SUA, we found that stimulus sensitivity for SUA was well predicted by the VEP in PF cortex but not in V4. Our results first reveal a functional specialization in both areas at the level of the LFP and further suggest that the degree to which mesoscopic signals, such as the VEP, are representative of the underlying SUA neural processing may be brain region specific within the context of visual recognition

Theta coupling between V4 and prefrontal cortex predicts visual short-term memory performance

Short-term memory requires communication between multiple brain regions that collectively mediate the encoding and maintenance of sensory information. It has been suggested that oscillatory synchronization underlies intercortical communication. Yet, whether and how distant cortical areas cooperate during visual memory remains elusive. We examined neural interactions between visual area V4 and the lateral prefrontal cortex using simultaneous local field potential (LFP) recordings and single- unit activity (SUA) in monkeys performing a visual short-term memory task. During the memory period, we observed enhanced between-area phase synchronization in theta frequencies (3–9 Hz) of LFPs together with elevated phase locking of SUA to theta oscillations across regions. In addition, we found that the strength of intercortical locking was predictive of the animals’ behavioral performance. This suggests that theta-band synchronization coordinates action potential communication between V4 and prefrontal cortex that may contribute to the maintenance of visual short-term memories