scholarly journals Precise timing is ubiquitous, consistent and coordinated across a comprehensive, spike-resolved flight motor program

2019 ◽  
Author(s):  
Joy Putney ◽  
Rachel Conn ◽  
Simon Sponberg

Sequences of action potentials, or spikes, carry information in the number of spikes and their timing. Spike timing codes are critical in many sensory systems, but there is now growing evidence that millisecond-scale changes in timing also carry information in motor brain regions, descending decision-making circuits, and individual motor units. Across all the many signals that control a behavior how ubiquitous, consistent, and coordinated are spike timing codes? Assessing these open questions ideally involves recording across the whole motor program with spike-level resolution. To do this, we took advantage of the relatively few motor units controlling the wings of a hawk moth, Manduca sexta. We simultaneously recorded nearly every action potential from all major wing muscles and the resulting forces in tethered flight. We found that timing encodes more information about turning behavior than spike count in every motor unit, even though there is sufficient variation in count alone. Flight muscles vary broadly in function as well as in the number and timing of spikes. Nonetheless, each muscle with multiple spikes consistently blends spike timing and count information in a 3:1 ratio. Coding strategies are consistent. Finally, we assess the coordination of muscles using pairwise redundancy measured through interaction information. Surprisingly, not only are all muscle pairs coordinated, but all coordination is accomplished almost exclusively through spike timing, not spike count. Spike timing codes are ubiquitous, consistent, and essential for coordination.Significance StatementBrains can encode precise sensory stimuli and specific motor systems also appear to be precise, but how important are millisecond changes in timing of neural spikes across the whole motor program for a behavior? We record every spike that the hawk moth’s nervous system sends to its wing muscles. We show that all muscles convey the majority of their information in spike timing. The number of spikes does play a role, but not in a coordinated way across muscles. Instead, all coordination is done using in the millisecond timing of in spikes. The importance and prevalence of timing across the motor program pose new questions for how nervous systems create precise, coordinated motor commands.

2019 ◽  
Vol 116 (52) ◽  
pp. 26951-26960 ◽  
Author(s):  
Joy Putney ◽  
Rachel Conn ◽  
Simon Sponberg

Sequences of action potentials, or spikes, carry information in the number of spikes and their timing. Spike timing codes are critical in many sensory systems, but there is now growing evidence that millisecond-scale changes in timing also carry information in motor brain regions, descending decision-making circuits, and individual motor units. Across all of the many signals that control a behavior, how ubiquitous, consistent, and coordinated are spike timing codes? Assessing these open questions ideally involves recording across the whole motor program with spike-level resolution. To do this, we took advantage of the relatively few motor units controlling the wings of a hawk moth,Manduca sexta. We simultaneously recorded nearly every action potential from all major wing muscles and the resulting forces in tethered flight. We found that timing encodes more information about turning behavior than spike count in every motor unit, even though there is sufficient variation in count alone. Flight muscles vary broadly in function as well as in the number and timing of spikes. Nonetheless, each muscle with multiple spikes consistently blends spike timing and count information in a 3:1 ratio. Coding strategies are consistent. Finally, we assess the coordination of muscles using pairwise redundancy measured through interaction information. Surprisingly, not only are all muscle pairs coordinated, but all coordination is accomplished almost exclusively through spike timing, not spike count. Spike timing codes are ubiquitous, consistent, and essential for coordination.


2019 ◽  
Author(s):  
Daniel J Denman ◽  
R Clay Reid

ABSTRACTSensory stimuli are represented by the joint activity of large populations of neurons across the mammalian cortex. Information in such responses is limited by trial-to-trial variability. Because that variability is not independent between neurons, it has the potential to improve or degrade the amount of sensory information in the population response. How visual information scales with population size remains an open empirical question. Here, we use Neuropixels to simultaneously record tens to hundreds of single neurons in primary visual cortex (V1) and lateral geniculate nucleus (LGN) of mice and estimate population information. We found a mix of synergistic and redundant coding: synergy predominated in small populations (2-12 cells) before giving way to redundancy. The shared variability of this coding regime included global shared spike count variability at longer timescales, layer specific shared spike count variability at finer timescales, and shared variability in spike timing (jitter) that linked ensembles that span layers. Such ensembles defined by their shared variability carry more information. Our results suggest fine time scale stimulus encoding may be distributed across physically overlapping but distinct ensembles in V1.


2002 ◽  
Vol 87 (4) ◽  
pp. 1749-1762 ◽  
Author(s):  
Shigeto Furukawa ◽  
John C. Middlebrooks

Previous studies have demonstrated that the spike patterns of cortical neurons vary systematically as a function of sound-source location such that the response of a single neuron can signal the location of a sound source throughout 360° of azimuth. The present study examined specific features of spike patterns that might transmit information related to sound-source location. Analysis was based on responses of well-isolated single units recorded from cortical area A2 in α-chloralose-anesthetized cats. Stimuli were 80-ms noise bursts presented from loudspeakers in the horizontal plane; source azimuths ranged through 360° in 20° steps. Spike patterns were averaged across samples of eight trials. A competitive artificial neural network (ANN) identified sound-source locations by recognizing spike patterns; the ANN was trained using the learning vector quantization learning rule. The information about stimulus location that was transmitted by spike patterns was computed from joint stimulus-response probability matrices. Spike patterns were manipulated in various ways to isolate particular features. Full-spike patterns, which contained all spike-count information and spike timing with 100-μs precision, transmitted the most stimulus-related information. Transmitted information was sensitive to disruption of spike timing on a scale of more than ∼4 ms and was reduced by an average of ∼35% when spike-timing information was obliterated entirely. In a condition in which all but the first spike in each pattern were eliminated, transmitted information decreased by an average of only ∼11%. In many cases, that condition showed essentially no loss of transmitted information. Three unidimensional features were extracted from spike patterns. Of those features, spike latency transmitted ∼60% more information than that transmitted either by spike count or by a measure of latency dispersion. Information transmission by spike patterns recorded on single trials was substantially reduced compared with the information transmitted by averages of eight trials. In a comparison of averaged and nonaveraged responses, however, the information transmitted by latencies was reduced by only ∼29%, whereas information transmitted by spike counts was reduced by 79%. Spike counts clearly are sensitive to sound-source location and could transmit information about sound-source locations. Nevertheless, the present results demonstrate that the timing of the first poststimulus spike carries a substantial amount, probably the majority, of the location-related information present in spike patterns. The results indicate that any complete model of the cortical representation of auditory space must incorporate the temporal characteristics of neuronal response patterns.


2005 ◽  
Vol 6 (1) ◽  
pp. 41-55 ◽  
Author(s):  
Miguel A. Herrero ◽  
José M. López

In this work we succintly review the main features of bone formation in vertebrates. Out of the many aspects of this exceedingly complex process, some particular stages are selected for which mathematical modelling appears as both feasible and desirable. In this way, a number of open questions are formulated whose study seems to require interaction among mathematical analysis and biological experimentation.


2008 ◽  
Vol 100 (1) ◽  
pp. 268-280 ◽  
Author(s):  
Guglielmo Foffani ◽  
John K. Chapin ◽  
Karen A. Moxon

Computational studies are challenging the intuitive view that neurons with broad tuning curves are necessarily less discriminative than neurons with sharp tuning curves. In the context of somatosensory processing, broad tuning curves are equivalent to large receptive fields. To clarify the computational role of large receptive fields for cortical processing of somatosensory information, we recorded ensembles of single neurons from the infragranular forelimb/forepaw region of the rat primary somatosensory cortex while tactile stimuli were separately delivered to different locations on the forelimbs/forepaws under light anesthesia. We specifically adopted the perspective of individual columns/segregates receiving inputs from multiple body location. Using single-trial analyses of many single-neuron responses, we obtained two main results. 1) The responses of even small populations of neurons recorded from within the same estimated column/segregate can be used to discriminate between stimuli delivered to different surround locations in the excitatory receptive fields. 2) The temporal precision of surround responses is sufficiently high for spike timing to add information over spike count in the discrimination between surround locations. This surround spike-timing code (i) is particularly informative when spike count is ambiguous, e.g., in the discrimination between close locations or when receptive fields are large, (ii) becomes progressively more informative as the number of neurons increases, (iii) is a first-spike code, and (iv) is not limited by the assumption that the time of stimulus onset is known. These results suggest that even though large receptive fields result in a loss of spatial selectivity of single neurons, they can provide as a counterpart a sophisticated temporal code based on latency differences in large populations of neurons without necessarily sacrificing basic information about stimulus location.


2007 ◽  
Vol 98 (4) ◽  
pp. 2232-2243 ◽  
Author(s):  
Alon Nevet ◽  
Genela Morris ◽  
Guy Saban ◽  
David Arkadir ◽  
Hagai Bergman

Previous studies of single neurons in the substantia nigra reticulata (SNr) have shown that many of them respond to similar events. These results, as well as anatomical studies, suggest that SNr neurons share inputs and thus may have correlated activity. Different types of correlation can exist between pairs of neurons. These are traditionally classified as either spike-count (“signal” and “noise”) or spike-timing (spike-to-spike and joint peristimulus time histograms) correlations. These measures of neuronal correlation are partially independent and have different implications. Our purpose was to probe the computational characteristics of the basal ganglia output nuclei through an analysis of these different types of correlation in the SNr. We carried out simultaneous multiple-electrode single-unit recordings in the SNr of two monkeys performing a probabilistic delayed visuomotor response task. A total of 113 neurons (yielding 355 simultaneously recorded pairs) were studied. Most SNr neurons responded to one or more task-related events, with instruction cue (69%) and reward (63%) predominating. Response-match analysis, comparing peristimulus time histograms, revealed a significant overlap between response vectors. However, no measure of average correlation differed significantly from zero. The lack of significant SNr spike-count population correlations appears to be an exceptional phenomenon in the brain, perhaps indicating unique event-related processing by basal ganglia output neurons to achieve better information transfer. The lack of spike-timing correlations suggests that the basal high-frequency discharge of SNr neurons is not driven by the common inputs and is probably intrinsic.


2011 ◽  
Vol 105 (4) ◽  
pp. 1889-1896 ◽  
Author(s):  
Andrew M. Rosen ◽  
Jonathan D. Victor ◽  
Patricia M. Di Lorenzo

Recent studies have provided evidence that temporal coding contributes significantly to encoding taste stimuli at the first central relay for taste, the nucleus of the solitary tract (NTS). However, it is not known whether this coding mechanism is also used at the next synapse in the central taste pathway, the parabrachial nucleus of the pons (PbN). In the present study, electrophysiological responses to taste stimuli (sucrose, NaCl, HCl, and quinine) were recorded from 44 cells in the PbN of anesthetized rats. In 29 cells, the contribution of the temporal characteristics of the response to the discrimination of various taste qualities was assessed. A family of metrics that quantifies the similarity of two spike trains in terms of spike count and spike timing was used. Results showed that spike timing in 14 PbN cells (48%) conveyed a significant amount of information about taste quality, beyond what could be conveyed by spike count alone. In another 14 cells (48%), the rate envelope (time course) of the response contributed significantly more information than spike count alone. Across cells there was a significant correlation ( r = 0.51; P < 0.01) between breadth of tuning and the proportion of information conveyed by temporal dynamics. Comparison with previous data from the NTS (Di Lorenzo PM and Victor JD. J Neurophysiol 90: 1418–31, 2003 and J Neurophysiol 97: 1857–1861, 2007) showed that temporal coding in the NTS occurred in a similar proportion of cells and contributed a similar fraction of the total information at the same average level of temporal precision, even though trial-to-trial variability was higher in the PbN than in the NTS. These data suggest that information about taste quality conveyed by the temporal characteristics of evoked responses is transmitted with high fidelity from the NTS to the PbN.


Author(s):  
Jill North

It is often claimed, or hoped, that some temporal asymmetries are explained by the thermodynamic asymmetry in time. Thermodynamics, the macroscopic physics of pressure, temperature, volume, and so on, describes many temporally asymmetric processes. Heat flows spontaneously from hot objects to cold objects (in closed systems), never the reverse. More generally, systems spontaneously move from non-equilibrium states to equilibrium states, never the reverse. Delving into the foundations of statistical mechanics, this chapter reviews the many open questions in that field as they relate to temporal asymmetry. Taking a stand on many of them, it tackles questions about the nature of probabilities, the role of boundary conditions, and even the nature and scope of statistical mechanics.


2011 ◽  
Vol 105 (1) ◽  
pp. 69-87 ◽  
Author(s):  
David M. Devilbiss ◽  
Barry D. Waterhouse

Neurons of the nucleus locus coeruleus (LC) discharge with phasic bursts of activity superimposed on highly regular tonic discharge rates. Phasic bursts are elicited by bottom-up input mechanisms involving novel/salient sensory stimuli and top-down decision making processes; whereas tonic rates largely fluctuate according to arousal levels and behavioral states. Although it is generally believed that these two modes of activity differentially modulate information processing in LC targets, the unique role of phasic versus tonic LC output on signal processing in cells, circuits, and neural networks of waking animals is not well understood. In the current study, simultaneous recordings of individual neurons within ventral posterior medial thalamus and barrel field cortex of conscious rats provided evidence that each mode of LC output produces a unique modulatory impact on single neuron responsiveness to sensory-driven synaptic input and representations of sensory information across ensembles of simultaneously recorded cells. Each mode of LC activation specifically modulated the relationship between sensory-stimulus intensity and the subsequent responses of individual neurons and neural ensembles. Overall these results indicate that phasic versus tonic modes of LC discharge exert fundamentally different modulatory effects on target neuronal circuits within the rodent trigeminal somatosensory system. As such, each mode of LC output may differentially influence signal processing as a means of optimizing behaviorally relevant neural computations within this sensory network. Likely the ability of the LC system to differentially regulate neural responses and local circuit operations according to behavioral demands extends to other brain regions including those involved in higher cognitive functions.


2014 ◽  
Vol 369 (1641) ◽  
pp. 20130534 ◽  
Author(s):  
Theofanis I. Panagiotaropoulos ◽  
Vishal Kapoor ◽  
Nikos K. Logothetis

The combination of electrophysiological recordings with ambiguous visual stimulation made possible the detection of neurons that represent the content of subjective visual perception and perceptual suppression in multiple cortical and subcortical brain regions. These neuronal populations, commonly referred to as the neural correlates of consciousness , are more likely to be found in the temporal and prefrontal cortices as well as the pulvinar, indicating that the content of perceptual awareness is represented with higher fidelity in higher-order association areas of the cortical and thalamic hierarchy, reflecting the outcome of competitive interactions between conflicting sensory information resolved in earlier stages. However, despite the significant insights into conscious perception gained through monitoring the activities of single neurons and small, local populations, the immense functional complexity of the brain arising from correlations in the activity of its constituent parts suggests that local, microscopic activity could only partially reveal the mechanisms involved in perceptual awareness. Rather, the dynamics of functional connectivity patterns on a mesoscopic and macroscopic level could be critical for conscious perception. Understanding these emergent spatio-temporal patterns could be informative not only for the stability of subjective perception but also for spontaneous perceptual transitions suggested to depend either on the dynamics of antagonistic ensembles or on global intrinsic activity fluctuations that may act upon explicit neural representations of sensory stimuli and induce perceptual reorganization. Here, we review the most recent results from local activity recordings and discuss the potential role of effective, correlated interactions during perceptual awareness.


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