Eye movements modulate activity in hippocampal, parahippocampal, and inferotemporal neurons

Ringo, James L.; Sobotka, Stanislaw; Diltz, Mark D.; Bunce, C. M.

doi:10.1152/jn.1994.71.3.1285

Cited by 120 publications

(82 citation statements)

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“…Based on this analysis, the spike patterns of 58 (44%) of 131 single units were predictable across individual saccades to a degree that was significantly greater than chance (test of proportions, P < 0.01). This proportion is in agreement with previously reported saccadic modulation in the monkey medial temporal lobe (MTL) (23,24). In addition, we compared the incidence of saccade-modulated neurons with that of neurons that were significantly responsive to the onset of visual stimuli (16), and we found no correlation between the two distributions (Spearman's rank correlation coefficient, ρ = 0.09; P > 0.1), indicating that the tendency of neurons to show saccade modulation was not simply a reflection of visual sensitivity.…”

Section: Resultssupporting

confidence: 93%

“…Because the timing of neuronal spikes in the hippocampus is influenced by theta oscillations (9,(44)(45)(46), theta phase resetting could represent a mechanism by which stimulus-related activity in the hippocampus, in the form of neuronal firing, may be coordinated with ongoing behavior to optimize memory formation. Previous studies of saccadic modulation in the primate hippocampus have drawn parallels between this modulation and theta activity in rodents (24,47). Saccadic eye movements partition sensory input into discrete elements in much the same way that whisking and sniffing, behaviors often associated with hippocampal theta in rodents, break up somatosensory and olfactory information, respectively (1).…”

Section: Discussionmentioning

confidence: 99%

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Oscillatory activity in the monkey hippocampus during visual exploration and memory formation

Jutras¹,

Fries

Buffalo

2013

Proc. Natl. Acad. Sci. U.S.A.

253

266

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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 ...

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Section: Resultssupporting

confidence: 93%

Section: Discussionmentioning

confidence: 99%

Oscillatory activity in the monkey hippocampus during visual exploration and memory formation

Jutras¹,

Fries

Buffalo

2013

Proc. Natl. Acad. Sci. U.S.A.

253

266

View full text Add to dashboard Cite

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“…Nevertheless, investigations of the effects of fiber-sparing neurotoxic lesion of these cortical areas will be necessary to ascertain whether or not the item-specific recognition impairment after areas TH/TF could be associated with indirect, even relatively small, transection of fibers traveling from visual areas V4 and TE to PRh more rostrally (Suzuki, 1996). In addition, given that saccadic eye movements (even in complete darkness) modulate TH/TF neuron activity (Ringo et al, 1994;Nowicka et al, 1995;Sobotka et al, 1997), it remains possible that the increase in saccadic eye movements found after TH/TF lesions could have affected the way in which the operated monkeys …”

Section: Parahippocampal Cortex (Th/tf) and Recognition Memorymentioning

confidence: 99%

The Hippocampal/Parahippocampal Regions and Recognition Memory: Insights from Visual Paired Comparison versus Object-Delayed Nonmatching in Monkeys

Nemanic¹,

Ospina-Alvarado²,

Bachevalier³

2004

J. Neurosci.

202

223

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Recognition memory was assessed by submitting the same adult monkeys to visual paired comparison (VPC) with mixed delays (10 -120 sec), followed by three consecutive versions of object-delayed nonmatching-to-sample (DNMS): increasing delays (10 -600 sec), lengthened lists (3-10 objects), and intervening distractors in the delays (light at 10 sec, motor task at 30 -600 sec, or context change at 600 sec). Four groups were tested: normal controls, monkeys with ibotenic acid lesions of the hippocampal formation (H), and monkeys with aspiration lesions of either the perirhinal (PRh) or parahippocampal (areas TH/TF) cortex. Group H was impaired on VPC at delays Ն60 sec but had difficulty on DNMS only at 600 sec delays with distraction. In group TH/TF, the VPC impairment emerged earlier (30 sec); yet, once the nonmatching rule was mastered, no significant change occurred on any DNMS condition. Only group PRh behaved congruently on VPC and DNMS, exhibiting a deficit at the easiest condition that worsened with increasing delays as well as in DNMS lengthened list and distraction conditions. These results led us to postulate that VPC and DNMS, as previously administered to monkeys, were not equivalent visual recognition memory probes. Specifically, we propose that, for VPC, because of passive (incidental) encoding, the animal's performance rests on both item familiarity and event recollection, whereas, for DNMS, because of active (purposeful) encoding, performance relies more on item familiarity. This proposal converges with current models postulating distinct, but interactive, mnemonic roles for the hippocampal and adjacent TH/TF regions.

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“…Ringo et al (1994) and Sobotka et al (1997) have described modulation by eye movement in the activity of the inferior and medial temporal cortical neurons. The work of Scheinberg and Logothetis (2001) has recently focused on natural vision (with its rich repertoire of SEM) and the activity of IT cells.…”

Section: Discussionmentioning

confidence: 99%

Modulation by context of a scene in monkey anterior inferotemporal cortex during a saccadic eye movement task

Lima¹,

Fiorani²,

Gattass³

2003

An. Acad. Bras. Ciênc.

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We investigated the effect of a scene on the activity of cells in the anterior inferotemporal (AIT) cortex while the monkey performed a saccadic eye movement (SEM) task with and without the context of a scene (gray frame). Most neurons did not code for the presence of a scene when it appeared alone (monkey free viewing) or when the monkey was fixating. Nevertheless, when a peripheral target was turned on and the monkey had to make a SEM to it, some cells were capable of differentially coding the presence of the scene before and after the saccade.

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Eye movements modulate activity in hippocampal, parahippocampal, and inferotemporal neurons

Cited by 120 publications

References 0 publications

Oscillatory activity in the monkey hippocampus during visual exploration and memory formation

Oscillatory activity in the monkey hippocampus during visual exploration and memory formation

The Hippocampal/Parahippocampal Regions and Recognition Memory: Insights from Visual Paired Comparison versus Object-Delayed Nonmatching in Monkeys

Modulation by context of a scene in monkey anterior inferotemporal cortex during a saccadic eye movement task

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