Behaviorally Relevant Burst Coding in Primary Sensory Neurons

Sabourin, Patrick; Pollack, Gerald S.

doi:10.1152/jn.00370.2009

Cited by 16 publications

(20 citation statements)

References 23 publications

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“…Indeed, there is a clear tendency for different HF receptors to fire in near synchrony, particularly when they produce bursts. This can be expected to result in strong depolarization of their target neurons, helping to ensure that they, too, respond with bursts (Sabourin and Pollack 2009). In this respect, HF receptors are well suited to participate in coincidence-detector-type processing, in contrast to MT receptors, which are better suited to an integrator-type circuit.…”

Section: Discussionmentioning

confidence: 99%

“…1E; three-way ANOVA, receptor-type effect, P Ͻ 0.001). The firing rate is generally higher in HF receptors (Imaizumi and Pollack 2001;Sabourin and Pollack 2009) and information in neural spike trains increases linearly with firing rate (Borst and Haag 2001); however, this does not account for the greater information content of HF receptor responses, which remains higher than that of MT receptors on a per-spike basis (Fig. 1F).…”

Section: Temporal Tuning Of On1 Is Apparent At the Level Of Subthreshmentioning

confidence: 98%

“…By this measure as well, the similarity of spike trains is much higher for HF receptors than that for MT receptors. We previously showed that HF receptors tend to fire in bursts (Sabourin and Pollack 2009). Both the high correlation between spike trains in Fig.…”

Section: Temporal Tuning Of On1 Is Apparent At the Level Of Subthreshmentioning

confidence: 99%

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Temporal Coding by Populations of Auditory Receptor Neurons

Sabourin

Pollack

2010

Journal of Neurophysiology

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Sabourin P, Pollack GS. Temporal coding by populations of auditory receptor neurons. J Neurophysiol 103: 1614 -1621, 2010. First published January 13, 2010 doi:10.1152/jn.00621.2009. Auditory receptor neurons of crickets are most sensitive to either low or high sound frequencies. Earlier work showed that the temporal coding properties of first-order auditory interneurons are matched to the temporal characteristics of natural low-and high-frequency stimuli (cricket songs and bat echolocation calls, respectively). We studied the temporal coding properties of receptor neurons and used modeling to investigate how activity within populations of low-and high-frequency receptors might contribute to the coding properties of interneurons. We confirm earlier findings that individual low-frequencytuned receptors code stimulus temporal pattern poorly, but show that coding performance of a receptor population increases markedly with population size, due in part to low redundancy among the spike trains of different receptors. By contrast, individual high-frequency-tuned receptors code a stimulus temporal pattern fairly well and, because their spike trains are redundant, there is only a slight increase in coding performance with population size. The coding properties of low-and high-frequency receptor populations resemble those of interneurons in response to low-and high-frequency stimuli, suggesting that coding at the interneuron level is partly determined by the nature and organization of afferent input. Consistent with this, the sound-frequency-specific coding properties of an interneuron, previously demonstrated by analyzing its spike train, are also apparent in the subthreshold fluctuations in membrane potential that are generated by synaptic input from receptor neurons. I N T R O D U C T I O NThe temporal structures of sensory signals often carry behaviorally important information and this is particularly evident in communication systems. For example, in many acoustically communicating animals, including birds, frogs, insects, and humans, information such as the species and individual identity of the signaler, or the signal's "message" (e.g., speech; Shannon et al. 1995), is carried by features such as the durations of sounds and of the intervals between them (Bradbury and Vehrencamp 1998). Sensory neurons are often tuned to these behaviorally relevant temporal features; they may respond most strongly to these features (rate code) or the structure of their spike trains may capture most accurately the timing of these stimulus components (time code; Pollack and Krahe 2009).Two classes of sound stimuli are particularly important for the behavior of crickets: conspecific songs and echolocation calls of insectivorous bats. Both types of stimulus consist of series of discrete sounds (sound pulses), but they differ in tempo. Pulse rates in echolocation calls span a wide range, increasing from 5 to 10 Hz when the bat is searching for a target to Ͼ100 Hz during the final approach to the prey (Jones and Rydell 2003). By contrast, ...

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Section: Discussionmentioning

confidence: 99%

Section: Temporal Tuning Of On1 Is Apparent At the Level Of Subthreshmentioning

confidence: 98%

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Temporal Coding by Populations of Auditory Receptor Neurons

Sabourin

Pollack

2010

Journal of Neurophysiology

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“…Instead, they are capable of rich intrinsic dynamics such as oscillations (Gray and Singer, 1989;Stopfer et al, 1997;Doiron et al, 2003a) and bursting (i.e. the firing of packets of action potentials followed by quiescence) (Lemon and Turner, 2000;Sherman, 2001;Swensen and Bean, 2003;Krahe and Gabbiani, 2004;Sabourin and Pollack, 2009). Although much is known about the intrinsic mechanisms that lead to burst firing (Wang and Rinzel, 1995;Izhikevich, 2000;Krahe and Gabbiani, 2004), the functional role of burst firing is less well understood.…”

Section: Cihr Author Manuscriptmentioning

confidence: 99%

Neural heterogeneities and stimulus properties affect burst coding in vivo

2010

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Many neurons tend to fire clusters of action potentials called bursts followed by quiescence in response to sensory input. While the mechanisms that underlie burst firing are generally well understood in vitro, the functional role of these bursts in generating behavioral responses to sensory input in vivo are less clear. Pyramidal cells within the electrosensory lateral line lobe (ELL) of weakly electric fish offer an attractive model system for studying the coding properties of burst firing, because the anatomy and physiology of the electrosensory circuitry are well understood, and the burst mechanism of ELL pyramidal cells has been thoroughly characterized in vitro. We investigated the coding properties of bursts generated by these cells in vivo in response to mimics of behaviorally relevant sensory input. We found that heterogeneities within the pyramidal cell population had quantitative but not qualitative effects on burst coding for the low frequency components of broadband time varying input. Moreover, spatially localized stimuli mimicking, for example, prey tended to elicit more bursts than spatially global stimuli mimicking conspecific-related stimuli. We also found small but significant correlations between burst attributes such as the number of spikes per burst or the interspike interval during the burst and stimulus attributes such as stimulus amplitude or slope. These correlations were much weaker in magnitude than those observed in vitro. More surprisingly, our results show that correlations between burst and stimulus attributes actually decreased in magnitude when we used low frequency stimuli that are expected to promote burst firing. We propose that this discrepancy is attributable to differences between ELL pyramidal cell burst firing under in vivo and in vitro conditions. Keywordsweakly electric fish; neural coding; information theory; burst firing Understanding the neural code remains a central problem in neuroscience. This understanding is in part complicated by the fact that neurons in the brain are highly CIHR Author Manuscript CIHR Author Manuscript CIHR Author Manuscriptheterogeneous (Bannister and Larkman, 1995a,b;Bastian and Nguyenkim, 2001;Häusser and Mel, 2003) and are not passive input-driven devices. Instead, they are capable of rich intrinsic dynamics such as oscillations (Gray and Singer, 1989;Stopfer et al., 1997;Doiron et al., 2003a) and bursting (i.e. the firing of packets of action potentials followed by quiescence) (Lemon and Turner, 2000;Sherman, 2001;Swensen and Bean, 2003;Krahe and Gabbiani, 2004;Sabourin and Pollack, 2009). Although much is known about the intrinsic mechanisms that lead to burst firing (Wang and Rinzel, 1995;Izhikevich, 2000;Krahe and Gabbiani, 2004), the functional role of burst firing is less well understood. Studies have shown that bursts of action potentials are critical for mediating cricket escape behavior in response to threatening stimuli (Marsat and Pollack, 2006). The function of burst firing is less well understood in vertebrates: a va...

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“…Burst firing is an important excitability property related to motor control in central pattern generators (CPGs) (Brocard et al, 2010;Selverston, 2010), to sensory information processing in visual and auditory centers (Reinagel et al, 1999;Eyherabide et al, 2008;Sabourin and Pollack, 2009), and is known to enhance signal detection in thalamocortical circuits (Steriade et al, 1993;Sherman, 2001).…”

Section: Introductionmentioning

confidence: 99%

Single Synapse Information Coding in Intraburst Spike Patterns of Central Pattern Generator Motor Neurons

Brochini¹,

Carelli²,

Pinto³

2011

J. Neurosci.

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Burst firing is ubiquitous in nervous systems and has been intensively studied in central pattern generators (CPGs). Previous works have described subtle intraburst spike patterns (IBSPs) that, despite being traditionally neglected for their lack of relation to CPG motor function, were shown to be cell-type specific and sensitive to CPG connectivity. Here we address this matter by investigating how a bursting motor neuron expresses information about other neurons in the network. We performed experiments on the crustacean stomatogastric pyloric CPG, both in control conditions and interacting in real-time with computer model neurons. The sensitivity of postsynaptic to presynaptic IBSPs was inferred by computing their average mutual information along each neuron burst. We found that details of input patterns are nonlinearly and inhomogeneously coded through a single synapse into the fine IBSPs structure of the postsynaptic neuron following burst. In this way, motor neurons are able to use different time scales to convey two types of information simultaneously: muscle contraction (related to bursting rhythm) and the behavior of other CPG neurons (at a much shorter timescale by using IBSPs as information carriers). Moreover, the analysis revealed that the coding mechanism described takes part in a previously unsuspected information pathway from a CPG motor neuron to a nerve that projects to sensory brain areas, thus providing evidence of the general physiological role of information coding through IBSPs in the regulation of neuronal firing patterns in remote circuits by the CNS.

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Behaviorally Relevant Burst Coding in Primary Sensory Neurons

Cited by 16 publications

References 23 publications

Temporal Coding by Populations of Auditory Receptor Neurons

Temporal Coding by Populations of Auditory Receptor Neurons

Neural heterogeneities and stimulus properties affect burst coding in vivo

Single Synapse Information Coding in Intraburst Spike Patterns of Central Pattern Generator Motor Neurons

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