Rates and Rhythms: A Synergistic View of Frequency and Temporal Coding in Neuronal Networks

Ainsworth, Matthew; Lee, Shane; Cunningham, Mark O.; Traub, Roger D.; Kopell, Nancy; Whittington, Miles A.

doi:10.1016/j.neuron.2012.08.004

Cited by 135 publications

(135 citation statements)

References 126 publications

Supporting

Mentioning

131

Contrasting

Order By: Relevance

“…Indeed, several studies probing the relation of population performance with population size reported that population information grows steadily with population size. This led to the hypothesis that in sufficiently large ensembles each neuron contributes independently to a population code (Gawne et al, 1996;Rolls et al, 1997;Reich et al, 2001;Quiroga et al, 2007) and that large populations may encode very high amounts of information (Abbott et al, 1996).…”

Section: Introductionmentioning

confidence: 99%

Neural Codes Formed by Small and Temporally Precise Populations in Auditory Cortex

2013

View full text Add to dashboard Cite

The encoding of sensory information by populations of cortical neurons forms the basis for perception but remains poorly understood. To understand the constraints of cortical population coding we analyzed neural responses to natural sounds recorded in auditory cortex of primates (Macaca mulatta). We estimated stimulus information while varying the composition and size of the considered population. Consistent with previous reports we found that when choosing subpopulations randomly from the recorded ensemble, the average population information increases steadily with population size. This scaling was explained by a model assuming that each neuron carried equal amounts of information, and that any overlap between the information carried by each neuron arises purely from random sampling within the stimulus space. However, when studying subpopulations selected to optimize information for each given population size, the scaling of information was strikingly different: a small fraction of temporally precise cells carried the vast majority of information. This scaling could be explained by an extended model, assuming that the amount of information carried by individual neurons was highly nonuniform, with few neurons carrying large amounts of information. Importantly, these optimal populations can be determined by a single biophysical marker-the neuron's encoding time scale-allowing their detection and readout within biologically realistic circuits. These results show that extrapolations of population information based on random ensembles may overestimate the population size required for stimulus encoding, and that sensory cortical circuits may process information using small but highly informative ensembles.

show abstract

Section: Introductionmentioning

confidence: 99%

Neural Codes Formed by Small and Temporally Precise Populations in Auditory Cortex

2013

View full text Add to dashboard Cite

show abstract

“…A sensory system can employ multiple types of codes (Ainsworth et al, 2012). For instance, the barn owl auditory system computes two sound localization cues, using a rate code for interaural level differences and a temporal code for interaural timing differences (Konishi, 1993).…”

Section: Introductionmentioning

confidence: 99%

Multiplexed temporal coding of electric communication signals in mormyrid fishes

Baker

Kohashi

Lyons-Warren

et al. 2013

Journal of Experimental Biology

View full text Add to dashboard Cite

SummaryThe coding of stimulus information into patterns of spike times occurs widely in sensory systems. Determining how temporally coded information is decoded by central neurons is essential to understanding how brains process sensory stimuli. Mormyrid weakly electric fishes are experts at time coding, making them an exemplary organism for addressing this question. Mormyrids generate brief, stereotyped electric pulses. Pulse waveform carries information about sender identity, and it is encoded into submillisecond-to-millisecond differences in spike timing between receptors. Mormyrids vary the time between pulses to communicate behavioral state, and these intervals are encoded into the sequence of interspike intervals within receptors. Thus, the responses of peripheral electroreceptors establish a temporally multiplexed code for communication signals, one consisting of spike timing differences between receptors and a second consisting of interspike intervals within receptors. These signals are processed in a dedicated sensory pathway, and recent studies have shed light on the mechanisms by which central circuits can extract behaviorally relevant information from multiplexed temporal codes. Evolutionary change in the anatomy of this pathway is related to differences in electrosensory perception, which appears to have influenced the diversification of electric signals and species. However, it remains unknown how this evolutionary change relates to differences in sensory coding schemes, neuronal circuitry and central sensory processing. The mormyrid electric communication pathway is a powerful model for integrating mechanistic studies of temporal coding with evolutionary studies of correlated differences in brain and behavior to investigate neural mechanisms for processing temporal codes.Key words: sub-millisecond timing differences, duration tuning, interval tuning, coincidence detection, anti-coincidence detection, delay line, temporal filter, weakly electric fish, electric organ discharge. Division of Biological Science, Graduate School of Science, Nagoya University, Nagoya, Japan *Author for correspondence (carlson.bruce@wustl.edu) THE JOURNAL OF EXPERIMENTAL BIOLOGY 2366 that links changes in neural circuitry to differences in behavior. From the perspective of the central nervous system, there is no difference between the electrosense and other modalities -all stimuli are represented as patterns of spiking. Therefore, the mechanisms by which mormyrids process temporally coded information are relevant to understanding basic principles for how any neural circuit can solve this problem.Electric signals in mormyrid fishes communicate sender identity and behavioral state Two components of electrocommunication: EOD and IPI Mormyrids produce an electric organ discharge (EOD) to communicate and actively sense their environment (Hopkins, 1986). These fish have three types of electroreceptors in their skin: mormyromasts are used for active sensing, ampullary receptors for passive sensing and knollenorgans for commun...

show abstract

“…The first pool is the readily releasable pool (RRP) and the other is the recycling pool (RP) (15), modeled with mass-action kinetics. Synaptic dynamics has been repeatedly used to describe changes in spike rates in neural network populations (16) and emergence of gamma oscillations (17). Furthermore network connectivity can also participate to define bursting or the oscillation frequency in neural networks (18,19).…”

mentioning

confidence: 99%

Robust network oscillations during mammalian respiratory rhythm generation driven by synaptic dynamics

Guerrier

Hayes

Fortin

et al. 2015

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

View full text Add to dashboard Cite

How might synaptic dynamics generate synchronous oscillations in neuronal networks? We address this question in the preBötzinger complex (preBötC), a brainstem neural network that paces robust, yet labile, inspiration in mammals. The preBötC is composed of a few hundred neurons that alternate bursting activity with silent periods, but the mechanism underlying this vital rhythm remains elusive. Using a computational approach to model a randomly connected neuronal network that relies on short-term synaptic facilitation (SF) and depression (SD), we show that synaptic fluctuations can initiate population activities through recurrent excitation. We also show that a two-step SD process allows activity in the network to synchronize (bursts) and generate a population refractory period (silence). The model was validated against an array of experimental conditions, which recapitulate several processes the preBötC may experience. Consistent with the modeling assumptions, we reveal, by electrophysiological recordings, that SF/SD can occur at preBötC synapses on timescales that influence rhythmic population activity. We conclude that nondeterministic neuronal spiking and dynamic synaptic strengths in a randomly connected network are sufficient to give rise to regular respiratory-like rhythmic network activity and lability, which may play an important role in generating the rhythm for breathing and other coordinated motor activities in mammals.central pattern generator | synaptic depression | mathematical modeling | numerical simulations | breathing C entral pattern generators (CPGs) are neuronal circuits that generate coordinated activity in the absence of sensory input (1). One such mammalian CPG, the preBötzinger complex (preBötC), gives rise to the eupneic respiratory rhythm (2, 3). Located in the medulla, the preBötC preserves a spontaneous respiratory-like rhythm when isolated in transverse slices, but the precise nature of the cellular and synaptic mechanisms underlying rhythmogenesis remains elusive (3-7). An early hypothesis was that the neuronal activity is driven by intrinsically bursting pacemaker neurons synchronized via excitatory synaptic connections (2,6,8,9). However, electrophysiological and modeling studies (7, 10-12) now suggest the rhythm emerges through stochastic activation of intrinsic currents conveyed by recurrent synaptic connections, without the need for pacemaker neurons (3,4,11,13,14). In either case, excitatory synapses are required for rhythm generation; the possibility that synaptic properties also underlie periodic burst initiation and termination is yet to be demonstrated.Synaptic transmission relies on the release of vesicles, which can be modulated at the presynaptic terminal. Synaptic depression (SD), based on vesicular release, consists of decaying release probability after sustained activity, which subsequently decreases excitability within the underlying connected network. Conversely, synaptic facilitation (SF) enhances vesicular release probability and promotes neuronal synchronizatio...

show abstract

Rates and Rhythms: A Synergistic View of Frequency and Temporal Coding in Neuronal Networks

Cited by 135 publications

References 126 publications

Neural Codes Formed by Small and Temporally Precise Populations in Auditory Cortex

Neural Codes Formed by Small and Temporally Precise Populations in Auditory Cortex

Multiplexed temporal coding of electric communication signals in mormyrid fishes

Robust network oscillations during mammalian respiratory rhythm generation driven by synaptic dynamics

Contact Info

Product

Resources

About