Spontaneous Fluctuations in Visual Cortical Responses Influence Population Coding Accuracy

Gutnisky, Diego; Beaman, Charles; Lew, Sergio E.; Dragoi, Valentin

doi:10.1093/cercor/bhv312

Cited by 32 publications

(38 citation statements)

References 105 publications

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“…However, pre-activation would likely correspond to a higher pre-stimulus response in regions that process a particular stimulus type, not lower as was seen here. Prior studies in early visual cortex in monkeys also showed that lower pre-stimulus activity is associated with 9 improved tuning and behavior (16,17,37). The results of the present study show that these faciliatory effects can be differentially focused in circuits associated with processing specific stimulus types in higher-level visual regions and in regions outside of visual cortex in humans.…”

supporting

confidence: 74%

Endogenous activity modulates stimulus and circuit-specific neural tuning and perception

Ward

Richardson

et al. 2019

Preprint

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Perception reflects not only input from the sensory periphery, but also the endogenous neural state when sensory inputs enter the brain. Whether endogenous neural states influence perception only through global mechanisms, such as arousal, or can also perception in a neural circuit and stimulus specific manner remains largely unknown. Intracranial recordings from 30 pre-surgical epilepsy patients showed that endogenous activity independently modulated the strength of trialby-trial neural tuning of different visual category-selective neural circuits. Furthermore, the same aspect of the endogenous activity that influenced tuning in a particular neural circuit also correlated with reaction time only for trials with the category of image that circuit was selective for. These results suggest that endogenous activity may influence neural tuning and perception through circuit-specific predictive coding processes.2 Main Text: Perception depends on not only sensory input, but also the neural and cognitive state when a stimulus is presented. Traditionally, this endogenous activity has been treated as random biological noise(1). However, studies in both humans and animals demonstrate that rather than being a noise process, endogenous activity reflects fluctuations of neural activity that influence neural processing in a behaviorally relevant manner. Specifically, endogenous fluctuations in neural activity influence both coarse aspects of the neural response to sensory input(2-5) and the behavioral response to that input(5-9). Endogenous activity has rich structure, reflecting the stimulus processing properties of the local neural circuitry(10), broad scale brain network architecture(11), and may reflect statistically optimal representations of the environment(12). Fuctuations in endogenous processes such as arousal(13-15) and alertness (16,17) can influence stimulus processing and behavior. Some theoretical accounts posit that fluctuations of endogenous activity can reflect predictive processes(18) that facilitate stimulus processing in a stimulus-specific manner. However, most studies have only examined nonspecific mechanisms, such as arousal and alertness(13-17). Thus, there is a dearth of empirical evidence testing whether endogenous processes can influence neural tuning and influence behavior in a circuit and stimulus-specific manner as required by models of predictive processing.Data were acquired from 30 human neurosurgical patients with implanted intracranial electroencephalography (iEEG) while they viewed images of faces, bodies, words, hammers, houses, and scrambled non-objects and performed a 1-back, repeat detection task. Stimuli were balanced across categories and presented in a random order to reduce any potential cognitive or strategic processes that might favor one stimulus over another. This allowed us to probe the relationship between endogenous activity, visual category tuning, and behavior separately for

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supporting

confidence: 74%

Endogenous activity modulates stimulus and circuit-specific neural tuning and perception

Ward

Richardson

et al. 2019

Preprint

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“…On the one hand, spontaneous depolarization brings neurons closer to threshold prior to the arrival of excitatory sensory input. Accordingly, some studies show that enhanced levels of prestimulus activity correspond to larger responses 46,[48][49][50] . On the other hand, spontaneous synaptic barrages reduce input resistance 19,51,52 and depress synapses [53][54][55] .…”

Section: Discussionmentioning

confidence: 99%

Network activity influences the subthreshold and spiking visual responses of pyramidal neurons in a three-layer cortex

Weßel

2016

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A primary goal of systems neuroscience is to understand cortical function, which typically involves studying spontaneous and sensory-evoked cortical activity. Mounting evidence suggests a strong and complex relationship between the ongoing and evoked state. To date, most work in this area has been based on spiking in populations of neurons. While advantageous in many respects, this approach is limited in scope; it records the activities of a minority of neurons, and gives no direct indication of the underlying subthreshold dynamics. Membrane potential recordings can fill these gaps in our understanding, but are difficult to obtain in vivo. Here, we record subthreshold cortical visual responses in the ex vivo turtle eye-attached whole-brain preparation, which is ideally-suited to such a study. In the absence of visual stimulation, the network is "synchronous"; neurons display network-mediated transitions between low-and high-conductance membrane potential states. The prevalence of these slow-wave transitions varies across turtles and recording sessions. Visual stimulation evokes similar highconductance states, which are on average larger and less reliable when the ongoing state is more synchronous. Responses are muted when immediately preceded by large, spontaneous high-conductance events. Evoked spiking is sparse, highly variable across trials, and mediated by concerted synaptic inputs that are in general only very weakly correlated with inputs to nearby neurons. Together, these results highlight the multiplexed influence of the cortical network on the spontaneous and sensory-evoked activity of individual cortical neurons.Spikes are fundamental to cortical function; they are the means by which individual neurons receive and transmit information, and are the unit of language for cortical ensembles that encode sensory information. Understandably, then, most studies of cortical sensory responses have focused on the spiking activities of (increasingly large) populations of neurons. One recurring theme in this vast body of literature is the rich relationship between ongoing and evoked activity. Yet the spike-based approach yields an incomplete picture of this relationship (and sensory cortex generally), for three reasons. First, it reveals the activity of a minority of neurons; most cells spike very rarely, if at all 1 , and of those that do, few have spike rates sufficient for certain analyses 2 (Figure 1a). Second, neuronal populations defined by the recording device's field of view are unlikely to represent complete cortical microcircuits (Figure 1b). (While the local field potential (LFP) is both easily obtained and less susceptible to the first issue, this signal too is ultimately defined by the device (Figure 1b).) Third, the purely suprathreshold view of cortex leaves certain important questions unanswered. For example, some competing hypotheses of cortical function are not easily distinguishable by the spiking statistics of small populations, but predict very different subthreshold dynamics for individual ne...

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“…Individual pattern probabilities during SA (grey screen) and nat movies appeared to be fairly similar, both visually and in terms of the JSD, whilst mG seemed to modulate pattern probabilities differently. The experimental design allowed for comparing SA recorded at different times during the experiment, which enabled us to account for different brain states or network excitability levels 5,8,13 . Particularly nat movies and S2 recorded in close temporal coherence (interleaved between stimulus repetitions) revealed a low divergence of pattern distributions with values comparable to divergences between SA recorded at early and late experimental phases.…”

Section: /16mentioning

confidence: 99%

“…In addition, it has been suggested 30, 32 that instead of pairwise correlations between spike trains, population FR fluctuations may be responsible for the different pattern distributions and that considering population rate dynamics over simply mean FR was required to account for FR statistics 36 and that fluctuations in ongoing activity play an important role in population FR 13 . There has been considerable research into this with different models 13,24,30,36,37 . Population dynamics, and population FR differences between the various stimulus regimes could be implicated in the observed divergences.…”

Section: /16mentioning

confidence: 99%

“…a drifting grating may be unlikely to be observed under grey screen (representing lack of stimulation) or a different type of stimulus 4 . It has been shown that activity of populations, discriminability and spiking reliability are contingent on both sensory inputs and internal states 3,13 . Spontaneous activity (SA), neural events present during quiescent wakefulness and passive attention, has been hypothesised to play a role in memory recall and consolidation, and in gating of sensory inputs 14,15 .…”

Section: Introductionmentioning

confidence: 99%

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Neural ensemble activity depends on stimulus type in mouse primary visual cortex

Tolkiehn

Schultz

2019

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Early cortical processing of visual information has long been investigated by describing the response properties such as receptive fields or orientation selectivity of individual neurons to moving gratings. However, thanks to recent technological advances, it has been become easier to record from larger neuronal populations which allow us to analyse the population responses to probe visual information processing at the population level. In the end, it is unlikely that sensory processing is a single-neuron effort but that of an entire population. Here we show how different stimulus types evoke distinct binary activity patterns (words) of simultaneous events on different sites in the anaesthetised mouse. Spontaneous activity and natural scenes indicated lower word distribution divergences than each to drifting gratings. Accounting for firing rate differences, spontaneous activity was linked to more unique patterns than stimulus-driven responses. Multidimensional scaling conveyed that pattern probability distributions clustered for spatial frequencies but not for directions. Further, drifting gratings modulated the Shannon entropy estimated on spatial patterns in a similar fashion as classical directional and spatial frequency tuning functions of neurons. This was supported by a distinct sublinear relationship between Shannon entropy and mean population firing rate. 14/16

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Spontaneous Fluctuations in Visual Cortical Responses Influence Population Coding Accuracy

Cited by 32 publications

References 105 publications

Endogenous activity modulates stimulus and circuit-specific neural tuning and perception

Endogenous activity modulates stimulus and circuit-specific neural tuning and perception

Network activity influences the subthreshold and spiking visual responses of pyramidal neurons in a three-layer cortex

Neural ensemble activity depends on stimulus type in mouse primary visual cortex

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