Attention to a stimulus enhances both neuronal responses and gamma frequency synchrony in visual area V4, both of which should increase the impact of attended information on downstream neurons. To determine whether gamma synchrony is common throughout the ventral stream, we recorded from neurons in the superficial and deep layers of V1, V2, and V4 in two rhesus monkeys. We found an unexpected striking difference in gamma synchrony in the superficial vs. deep layers. In all three areas, spike-field coherence in the gamma (40-60 Hz) frequency range was largely confined to the superficial layers, whereas the deep layers showed maximal coherence at low frequencies (6-16 Hz), which included the alpha range. In the superficial layers of V2 and V4, gamma synchrony was enhanced by attention, whereas in the deep layers, alpha synchrony was reduced by attention. Unlike these major differences in synchrony, attentional effects on firing rates and noise correlation did not differ substantially between the superficial and deep layers. The results suggest that synchrony plays very different roles in feedback and feedforward projections. electrophysiology | macaque | oscillation A natomical and physiological studies have characterized the afferent inputs to and efferent inputs from neurons in different layers of visual cortical areas. However, physiological distinctions across layers, such as synchronous interactions, have not been fully identified. We first came across laminar differences in synchrony serendipitously. Gamma-band synchrony, measured either by spike-field or spike-spike interactions across multiple electrodes, is a prominent feature in visual cortex, and several studies have shown that attention enhances gamma-band synchrony in area V4 (1-5). In our first recordings in area V1, we also found prominent gamma-band synchrony, although the effects of attention, if any, were much smaller than what we previously found in V4 (1). However, in our first recordings in area V2 in the lunate sulcus, we were surprised to find hardly any gamma-band synchrony. We initially had no explanation for why V2 should be so different from V1 and V4. Probing at greater electrode depths led to the discovery that V2 cells do show gamma-band synchrony but only at those deeper electrode depths. Because V2 in the lunate sulcus bends under V1, layer 6 cells are closer to V1 on the occipital surface than are layer 1 cells. Thus, our deeper electrode recordings were actually located in the more superficial layers of V2. Because we typically studied the first responsive cells found in any penetration, this must have strongly biased our first recordings in V2 to the deep layers, and these deep layers apparently had little gamma-band synchrony. Conversely, the same tendency to sample the first responsive cells on a penetration would have resulted in a strong bias to record cells in the superficial layers of V1 and V4, from which we recorded directly on the cortical surface. This possibility led us to test whether the deep layers of V1 and V4 were...
Place-modulated activity among neurons in the hippocampal formation presents a means to organize contextual information in the service of memory formation and recall1,2. One particular spatial representation, that of grid cells, has been observed in the entorhinal cortex (EC) of rats and bats3–5, but has yet to be described in single units in primates. Here, we examined spatial representations in the EC of head-fixed monkeys performing a free-viewing visual memory task6,7. Individual neurons were identified in the primate EC that emitted action potentials when the monkey fixated multiple discrete locations in the visual field across the presentation of up to hundreds of novel images. These firing fields possess spatial periodicity similar to a triangular tiling with a corresponding well-defined hexagonal structure in the spatial autocorrelation. Further, these neurons demonstrated theta-band oscillatory activity and changing spatial scale as a function of distance from the rhinal sulcus, which is consistent with previous findings in rodents4,8–10. These spatial representations may provide a framework to anchor the encoding of stimulus content in a complex visual scene. Together, our results provide a direct demonstration of grid cells in the primate and suggest that EC neurons encode space during visual exploration, even without locomotion.
Monkeys with lesions limited to the hippocampal region (the hippocampus proper, the dentate gyrus, and the subiculum) were impaired on two tasks of recognition memory: delayed nonmatching to sample and the visual paired-comparison task. Recognition memory was impaired in five different groups of monkeys, whether the lesions were made by an ischemic procedure, by radio frequency, or by ibotenic acid. The finding that the hippocampal region is essential for normal recognition memory performance is considered in the context of current ideas about the role of the hippocampus in declarative memory.
Primates explore the visual world through the use of saccadic eye movements. Neuronal activity in the hippocampus, a structure known to be essential for memory, is modulated by this saccadic activity, but the relationship between visual exploration through saccades and memory formation is not well understood. Here, we identify a link between theta-band (3-12 Hz) oscillatory activity in the hippocampus and saccadic activity in monkeys performing a recognition memory task. As monkeys freely explored novel images, saccades produced a theta-band phase reset, and the reliability of this phase reset was predictive of subsequent recognition. In addition, enhanced theta-band power before stimulus onset predicted stronger stimulus encoding. Together, these data suggest that hippocampal theta-band oscillations act in concert with active exploration in the primate and possibly serve to establish the optimal conditions for stimulus encoding.T he use of saccadic eye movements to acquire information about the surrounding environment is perhaps the most conspicuous example of exploratory behavior in the primate. This behavior provides a mechanism for parsing incoming information into discrete, stable segments (i.e., snapshots of individual elements comprising a complex visual scene, allowing time for sufficient processing to occur before moving to the next fixation target). This mechanism of actively sampling sensory information from the environment may be similar to the behaviors engaged in by rodents exploring their environment through such activities as sniffing and whisking. Specifically, the fixation period following each saccade may be homologous to the period of incoming sensory information accompanying each sniff cycle in the rodent (1). Recently, it has been suggested that motor behaviors associated with information gathering are integral to the "active sensing" process in natural behavior (2). It is plausible that there may exist certain common neuronal elements across species that are associated with active sensing processes, such that the neuronal mechanisms underlying the encoding of information are intimately connected with the motor activities involved in acquiring that information.In many mammalian species, voluntary, exploratory behaviors are often associated with theta-band activity, a prominent 3-to 12-Hz oscillatory activity in the hippocampus and other limbic structures. This activity has been studied extensively in the rodent hippocampus (3-5), but it has also been described in bats (6), cats (7), and, more recently, humans (8-11). In rodents, theta appears to show close temporal relationships with running (3, 12) and sniffing (13), suggesting an association between theta and the rate of sensory input. Although hippocampal theta has been identified in anesthetized monkeys (14), the lack of a clear demonstration of hippocampal theta in awake monkeys has been attributed to the fact that the recording methods typically require immobile, head-affixed monkeys, in contrast to rodent studies using freely moving ...
Perirhinal cortex and area TE are immediately adjacent to each other in the temporal lobe and reciprocally interconnected. These areas are thought to lie at the interface between visual perception and visual memory, but it has been unclear what their separate contributions might be. In three experiments, monkeys with bilateral lesions of the perirhinal cortex exhibited a different pattern of impairment than monkeys with bilateral lesions of area TE. In experiment 1, lesions of the perirhinal cortex produced a multimodal deficit in recognition memory (delayed nonmatching to sample), whereas lesions of area TE impaired performance only in the visual modality. In experiment 2, on a test of visual recognition memory (the visual paired comparison task) lesions of the perirhinal cortex impaired performance at long delays but spared performance at a very short delay. In contrast, lesions of area TE impaired performance even at the short delay. In experiment 3, lesions of the perirhinal cortex and lesions of area TE produced an opposite pattern of impairment on two visual discrimination tasks, simple object discrimination learning (impaired only by perirhinal lesions), and concurrent discrimination learning (impaired only by TE lesions). Taken together, the findings suggest that the perirhinal cortex, like other medial temporal lobe structures, is important for the formation of memory, whereas area TE is important for visual perceptual processing.
Summary Selective visual attention is subserved by selective neuronal synchronization, entailing precise orchestration among excitatory and inhibitory cells. We tentatively identified these as broad (BS) and narrow spiking (NS) cells and analyzed their synchronization to the local field potential in two macaque monkeys performing a selective visual attention task. Across cells, gamma phases scattered widely but were unaffected by stimulation or attention. During stimulation, NS cells lagged BS cells on average by ~60° and gamma synchronized twice as strongly. Attention enhanced and reduced the gamma locking of strongly and weakly activated cells, respectively. During a pre-stimulus attentional cue period, BS cells showed weak gamma synchronization, while NS cells gamma synchronized as strongly as with visual stimulation. These analyses reveal the cell-type specific dynamics of the gamma cycle in macaque visual cortex and suggest that attention affects neurons differentially depending on cell type and activation level.
The visual processing of behaviorally relevant stimuli is enhanced through top-down attentional feedback. One possibility is that feedback targets early visual areas first and the attentional enhancement builds up at progressively later stages of the visual hierarchy. An alternative possibility is that the feedback targets the higher-order areas first and the attentional effects are communicated "backward" to early visual areas. Here, we compared the magnitude and latency of attentional enhancement of firing rates in V1, V2, and V4 in the same animals performing the same task. We found a reverse order of attentional effects, such that attentional enhancement was larger and earlier in V4 and smaller and later in V1, with intermediate results in V2. These results suggest that attentional mechanisms operate via feedback from higher-order areas to lower-order ones.attention | Macaque | vision | feedback N europhysiologic and brain imaging studies in monkeys and humans have shown that attended stimuli evoke larger responses in visual cortex than unattended distracters (1-6), giving attended stimuli a competitive advantage for representation in the cortex (7). These top-down attentional effects are thought to be mediated in part by feedback from prefrontal and posterior parietal cortex (8-12) acting directly or indirectly on all visual areas in the dorsal and ventral stream, including V1. However, the mechanism of this feedback is unclear. In particular, a first-order question is whether the top-down feedback targets V1 [or even the lateral geniculate nucleus (LGN)] first and then is passed on successively to later areas, or whether it targets higher-order areas first and then is fed back to successively lower areas. Without an understanding of the basic functional anatomy of the attentional feedback, it will be difficult to make progress in unraveling the circuitry for attention.The magnitude and timing of attentional effects on visual responses in all of the different visual structures should, in principle, give insight into the direction of attentional effects along the visual pathways. However, a comparison of the magnitude of attentional effects across visual areas in different studies leads to a confusing picture. On the one hand, imaging studies in humans typically find that attentional effects on evoked responses become larger as one moves from V1 into higher-order areas (13,14). Several neurophysiologic studies in monkeys also often report small (4) or even nonexistent (6, 15, 16) attentional enhancement of firing rates to stimuli in the receptive fields (RFs) of V1 cells (17-19), compared with reliable findings of attentional effects in higher-order areas such as V4 in conventional target detection or discrimination paradigms. On the other hand, other primate studies report substantial attentional effects in V1 in complex tasks such as covertly tracking along curved lines with spatially directed attention (18). It has recently been demonstrated that even with a relatively simple selection task, very large at...
More than 50 years of research have led to the general agreement that the hippocampus contributes to memory, but there has been a major schism among theories of hippocampal function over this time. Some researchers argue that the hippocampus plays a broad role in episodic and declarative memory, whereas others argue for a specific role in the creation of spatial cognitive maps and navigation. Although both views have merit, neither provides a complete account of hippocampal function. Guided by recent reviews that attempt to bridge between these views, here we suggest that reconciliation can be accomplished by exploring hippocampal function from the perspective of Tolman's (1948) original conception of a cognitive map as organizing experience and guiding behavior across all domains of cognition. We emphasize recent studies in animals and humans showing that hippocampal networks support a broad range of domains of cognitive maps, that these networks organize specific experiences within the contextually relevant map, and that network activity patterns reflect behavior guided through cognitive maps. These results are consistent with a framework that bridges theories of hippocampal function by conceptualizing the hippocampus as organizing incoming information within the context of a multidimensional cognitive map of spatial, temporal, and associational context.
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