Spatial Attention and Temporal Expectation Under Timed Uncertainty Predictably Modulate Neuronal Responses in Monkey V1

Sharma, Jitendra; Sugihara, Hiroki; Katz, Yarden; Schummers, James; Tenenbaum, Joshua; Sur, Mriganka

doi:10.1093/cercor/bhu086

Cited by 30 publications

(42 citation statements)

References 85 publications

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“…Consistent with prior studies of attentional modulation of firing rate in V1, we find modest facilitation of neuronal firing rates with attention [2, 3, 11–15, 22, 25–27, 30–32]. Attentional modulation of firing rate among V1 complex neurons was significantly greater than attentional modulation of firing rate among simple neurons, which were suppressed by attention on average (Figures 3A–B).…”

Section: Discussionsupporting

confidence: 90%

“…For complex neurons, AIs were calculated using the full 1-second analysis window, the first 250 msec (the “transient” window), and the last 250 msec (the “end” window). There were no differences in AI values across the different analysis windows used (p=0.7; see STAR Methods for details) so we chose the window that produced the largest AI for each complex neuron based on the rationale that neurons may be transiently modulated by attention [27]. Complex neurons with negative AI values had consistently negative AIs across analysis windows.…”

Section: Resultsmentioning

confidence: 99%

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Attentional Modulation of Neuronal Activity Depends on Neuronal Feature Selectivity

2017

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Attention exerts a powerful influence on visual perception. The impact of attention on neuronal activity manifests at early visual information processing stages and progressively increases throughout the visual cortical hierarchy. However, the neuronal mechanisms of attention are unresolved. In particular, the rules governing attentional modulation of individual neurons, whether they are facilitated or suppressed by attention, are not known. To obtain a more granular or neuron- and circuit-level understanding of the mechanisms of attention, and to directly test the feature similarity gain model in V1, we compared attentional modulation with neuronal feature selectivity across a large population of V1 neurons in alert and behaving macaque monkeys trained on an attention-demanding contrast-change detection task. We utilized emerging multi-electrode array technology to record simultaneously from V1 neurons spanning all 6 cortical layers so that we could characterize the laminar position and physiological response properties of diverse V1 neuronal populations. We found significant relationships between attentional modulation and neuronal position within the cortical hierarchy, neuronal physiology, and neuronal feature selectivity. Our results support the feature similarity gain model and further suggest that attentional modulation depends critically upon the match between neuronal feature selectivity and the features required for the task.

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Section: Discussionsupporting

confidence: 90%

Section: Resultsmentioning

confidence: 99%

Attentional Modulation of Neuronal Activity Depends on Neuronal Feature Selectivity

2017

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“…For the brain, the estimation of event occurrence is influenced by two main sources of uncertainty: first, by the actual probability distribution of events and second, by the brain's inherent uncertainty in estimating elapsed time (1,2). In previous work, ranging from single-cell recordings (3)(4)(5)(6)(7) to noninvasive electrophysiology (8,9) and neuroimaging (10,11), systems neuroscience has provided two compelling hypotheses for the computations involved in the neural representation of both sources of uncertainty.…”

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confidence: 99%

“…Hypothesis B assumes that the brain's uncertainty in estimating elapsed time is increasing monotonically with time, which is often referred to as the scalar property of time estimation (17,18). At the behavioral level (5,6,13) and at the neural level (3,(5)(6)(7)19), this uncertainty is typically modeled as a Gaussian function whose variance increases with elapsed time, a computation which is termed here as temporal blurring. Critically, temporal blurring ignores potential effects of environmental temporal statistics on time estimation, which raises the question whether the brain's estimation of time is influenced directly by event probability.…”

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confidence: 99%

The Anticipation of Events in Time

Grabenhorst

Michalareas

Maloney³

et al. 2019

Preprint

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Humans use sensory input to anticipate events. The brain's capacity to predict cues in time is commonly assumed to be modulated by two uncertainty parameters, the hazard rate (HR) of event probability and the uncertainty in time estimation, which increases with elapsed time.We investigate both assumptions by manipulating event probability density functions (PDF) in three sensory modalities. First we show, contrary to expectation, that perceptual systems use the reciprocal PDF -and not the HR -to model event probability density. Next we demonstrate that temporal uncertainty does not necessarily grow with elapsed time but also diminishes, depending on the event PDF. Finally we show that reaction time (RT) distributions comprise modality-specific and modality-independent components, the latter likely reflecting similarity in processing of probability density across sensory modalities. The results are consistent across vision, audition, and somatosensation, indicating that probability density is more fundamental than hazard rate in terms of the neural operations determining event anticipation and temporal uncertainty. Previous research identified neuronal activitity related to event probability in multiple levels of the cortical hierarchy such as early and higher sensory (V1, V4), association (LIP), motor and other areas. This work proposed that the elementary neuronal computation in estimation of probability across time is the HR. In contrast, our results suggest that the neurobiological implementation of probability estimation is based on a different, much simpler and more stable computation than HR: the reciprocal PDF of events in time.

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“…Foreperiod effects have already been demonstrated in a primate model (Sharma et al 2015), but the effects of cholinergic agents on temporal expectation in primates has not yet been investigated. In our experiment, the foreperiod effect on RT was eliminated by the scopolamine treatment.…”

Section: Discussionmentioning

confidence: 99%

Dissociating cholinergic influence on alertness and temporal attention in primates in a simple reaction time paradigm

Oláh

Knakker

Trunk

et al. 2019

Preprint

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Running titleCholinergic modulation of temporal attention in macaques Total number of pages 35 Total number of words in whole manuscript: 8167 text body (excl. Title Page, Abstract and Refences): 6276 Abstract: 234 AbstractThe ability to promptly respond to behaviourally relevant events depends on both general alertness and phasic changes in attentional state driven by temporal expectations. Using a variable foreperiod simple reaction time (RT) task in four adult male rhesus macaques, we investigated the role of the cholinergic system in alertness and temporal expectation.Foreperiod-effects on RT reflect temporal expectation, while alertness is quantified as overall response speed. We measured these RT parameters under vehicle treatment and systemic administration of the muscarinic receptor antagonist scopolamine. We also investigated whether and to what extent the effects of scopolamine were reversed by donepezil, a cholinesterase inhibitor widely used for the treatment of dementia. In the control condition, RT showed a continuous decrease as the foreperiod duration increased, which clearly indicated the effect of temporal expectation on RT. This foreperiod effect was detectable only on the faster tail of the RT distribution and was completely eliminated by scopolamine. Furthermore, scopolamine treatment slowed down the average RT. Donepezil treatment was efficient on the slower tail of the RT distribution and only improved the scopolamine induced impairments on average RT reflecting a beneficial effect on alertness without any improvement in temporal expectation. The present results highlight the role of the cholinergic system in temporal expectation and alertness in primates, and help delineate the efficacy and scope of donepezil and other cholinomimetic agents as cognitive enhancers in present and future clinical practice.

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Spatial Attention and Temporal Expectation Under Timed Uncertainty Predictably Modulate Neuronal Responses in Monkey V1

Cited by 30 publications

References 85 publications

Attentional Modulation of Neuronal Activity Depends on Neuronal Feature Selectivity

Attentional Modulation of Neuronal Activity Depends on Neuronal Feature Selectivity

The Anticipation of Events in Time

Dissociating cholinergic influence on alertness and temporal attention in primates in a simple reaction time paradigm

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