Parallel Coding of First- and Second-Order Stimulus Attributes by Midbrain Electrosensory Neurons

McGillivray, Patrick; Vonderschen, Katrin; Fortune, Eric S.; Chacron, Maurice J.

doi:10.1523/jneurosci.0478-12.2012

Cited by 63 publications

(108 citation statements)

References 90 publications

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“…It is likely that higher brain areas decode information about second-order attributes carried by correlated electroreceptor activity because weakly electric fish display strong and reliable behavioral responses to these attributes (13). Indeed, pyramidal cells within the electrosensory lateral line lobe strongly respond to envelopes at the single-neuron level (36) presumably through nonlinear integration of afferent synaptic input (26). In the vestibular system, neurons within the vestibular nuclei also nonlinearly integrate convergent vestibular afferent input (16) and are thus expected to strongly respond to the envelopes found in natural vestibular stimuli (17).…”

Section: Discussionmentioning

confidence: 99%

Coding of envelopes by correlated but not single-neuron activity requires neural variability

Metzen

Jamali

Carriot

et al. 2015

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

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Understanding how the brain processes sensory information is often complicated by the fact that neurons exhibit trial-to-trial variability in their responses to stimuli. Indeed, the role of variability in sensory coding is still highly debated. Here, we examined how variability influences neural responses to naturalistic stimuli consisting of a fast time-varying waveform (i.e., carrier or first order) whose amplitude (i.e., envelope or second order) varies more slowly. Recordings were made from fish electrosensory and monkey vestibular sensory neurons. In both systems, we show that correlated but not single-neuron activity can provide detailed information about second-order stimulus features. Using a simple mathematical model, we made the strong prediction that such correlation-based coding of envelopes requires neural variability. Strikingly, the performance of correlated activity at predicting the envelope was similarly optimally tuned to a nonzero level of variability in both systems, thereby confirming this prediction. Finally, we show that second-order sensory information can only be decoded if one takes into account joint statistics when combining neural activities. Our results thus show that correlated but not single-neural activity can transmit information about the envelope, that such transmission requires neural variability, and that this information can be decoded. We suggest that envelope coding by correlated activity is a general feature of sensory processing that will be found across species and systems. correlation | envelope | electrosensory | vestibular | neural coding A lthough correlated activity and neural variability are both observed ubiquitously in the brain, their functional roles have been the focus of much debate (1, 2). Indeed, the conventional wisdom that both are detrimental to coding by introducing redundancy and noise, respectively, has been recently challenged (3, 4). Here, we investigated the effects of variability on the coding by correlated activity of naturalistic sensory stimuli that often have rich spatiotemporal structure characterized by firstand second-order attributes. Specifically, we considered how neural populations within the electrosensory system of weakly electric fish and the vestibular system of monkeys respond to stimuli consisting of a fast time-varying carrier waveform (i.e., first-order attribute) whose amplitude or envelope (i.e., secondorder attribute) varies independently on a longer timescale. Envelopes are critical for perception (5, 6), yet their neural encoding continues to pose a challenge to investigators because they are nonlinearly related to the stimulus waveform (7). Previous studies have shown that single neurons can transmit envelope information through changes in firing rate (8, 9) when the relationship between the stimulus input and the output firing rate is nonlinear. In contrast, here, we focused on neuronal responses that were linearly related to the stimulus waveform.Weakly electric fish generate an electric field around their body throug...

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Section: Discussionmentioning

confidence: 99%

Coding of envelopes by correlated but not single-neuron activity requires neural variability

Metzen

Jamali

Carriot

et al. 2015

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

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“…Indeed, McGillivray and colleagues (McGillivray et al, 2012) showed that, while all pyramidal cells respond to both AMs and envelopes, superficial pyramidal cells tend to respond most strongly to envelopes while deep pyramidal cells tend to respond least strongly to envelopes (Fig.7B). This is because superficial pyramidal cells, with their low baseline firing rates, tend to display the most cut-off in response to AMs (Fig.7C).…”

Section: Coding In Electric Fishmentioning

confidence: 91%

“…While it has been known for some time that pyramidal cells respond to envelopes (Middleton et al, 2006), recent experiments have shown a large heterogeneity in these responses (Marsat and Maler, 2010;McGillivray et al, 2012). Indeed, McGillivray and colleagues (McGillivray et al, 2012) showed that, while all pyramidal cells respond to both AMs and envelopes, superficial pyramidal cells tend to respond most strongly to envelopes while deep pyramidal cells tend to respond least strongly to envelopes (Fig.7B).…”

Section: Coding In Electric Fishmentioning

confidence: 96%

“…In general, the depth of modulation is proportional to the distance of an object or conspecific from electroreceptors in the skin of an individual fish. The envelope, which is described in detail below, is the timevarying modulation of the depth of modulation of the AM and is a function of multiple environmental variables (Middleton et al, 2006;Middleton et al, 2007;Longtin et al, 2008;Savard et al, 2011;McGillivray et al, 2012;Stamper et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

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Perception and coding of envelopes in weakly electric fishes

Stamper

Fortune

Chacron

2013

Journal of Experimental Biology

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Summary Natural sensory stimuli have a rich spatiotemporal structure and can often be characterized as a high frequency signal that is independently modulated at lower frequencies. This lower frequency modulation is known as the envelope. Envelopes are commonly found in a variety of sensory signals, such as contrast modulations of visual stimuli and amplitude modulations of auditory stimuli. While psychophysical studies have shown that envelopes can carry information that is essential for perception, how envelope information is processed in the brain is poorly understood. Here we review the behavioral salience and neural mechanisms for the processing of envelopes in the electrosensory system of wave-type gymnotiform weakly electric fishes. These fish can generate envelope signals through movement, interactions of their electric fields in social groups or communication signals. The envelopes that result from the first two behavioral contexts differ in their frequency content, with movement envelopes typically being of lower frequency. Recent behavioral evidence has shown that weakly electric fish respond in robust and stereotypical ways to social envelopes to increase the envelope frequency. Finally, neurophysiological results show how envelopes are processed by peripheral and central electrosensory neurons. Peripheral electrosensory neurons respond to both stimulus and envelope signals. Neurons in the primary hindbrain recipient of these afferents, the electrosensory lateral line lobe (ELL), exhibit heterogeneities in their responses to stimulus and envelope signals. Complete segregation of stimulus and envelope information is achieved in neurons in the target of ELL efferents, the midbrain torus semicircularis (Ts).

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“…In these groups, the complex interaction of electric fields can give rise to modulations called envelopes (Stamper et al, 2013), through the relative movement between individuals (Yu et al, 2012), or the higher order interaction of their EODs (Stamper et al, 2012). Evidence of envelope processing has been revealed in the electrosensory system in weakly electric fish (Middleton et al, 2006;Longtin et al, 2008;McGillivray et al, 2012;Savard et al, 2011). In addition, Eigenmannia have a behavioral response to lowfrequency 'social envelopes' (Stamper et al, 2012).…”

Section: Refining and Extending The Modelmentioning

confidence: 99%

Closed-loop stabilization of the jamming avoidance response reveals its locally unstable and globally nonlinear dynamics

Madhav

Stamper

Fortune

et al. 2013

Journal of Experimental Biology

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SUMMARYThe Jamming Avoidance Response, or JAR, in the weakly electric fish has been analyzed at all levels of organization, from wholeorganism behavior down to specific ion channels. Nevertheless, a parsimonious description of the JAR behavior in terms of a dynamical system model has not been achieved at least in part due to the fact that 'avoidance' behaviors are both intrinsically unstable and nonlinear. We overcame the instability of the JAR in Eigenmannia virescens by closing a feedback loop around the behavioral response of the animal. Specifically, the instantaneous frequency of a jamming stimulus was tied to the fish's own electrogenic frequency by a feedback law. Without feedback, the fish's own frequency diverges from the stimulus frequency, but appropriate feedback stabilizes the behavior. After stabilizing the system, we measured the responses in the fish's instantaneous frequency to various stimuli. A delayed first-order linear system model fitted the behavior near the equilibrium. Coherence to white noise stimuli together with quantitative agreement across stimulus types supported this local linear model. Next, we examined the intrinsic nonlinearity of the behavior using clamped frequency difference experiments to extend the model beyond the neighborhood of the equilibrium. The resulting nonlinear model is composed of competing motor return and sensory escape terms. The model reproduces responses to step and ramp changes in the difference frequency (df) and predicts a 'snap-through' bifurcation as a function of dF that we confirmed experimentally.

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Parallel Coding of First- and Second-Order Stimulus Attributes by Midbrain Electrosensory Neurons

Cited by 63 publications

References 90 publications

Coding of envelopes by correlated but not single-neuron activity requires neural variability

Coding of envelopes by correlated but not single-neuron activity requires neural variability

Perception and coding of envelopes in weakly electric fishes

Closed-loop stabilization of the jamming avoidance response reveals its locally unstable and globally nonlinear dynamics

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