Sequential Filtering Processes Shape Feature Detection in Crickets: A Framework for Song Pattern Recognition.

Intraspecific acoustic communication requires filtering processes and feature detectors in the auditory pathway of the receiver for the recognition of species-specific signals. Insects like acoustically communicating crickets allow describing and analysing the mechanisms underlying auditory processing at the behavioral and neural level. Female crickets approach male calling song, their phonotactic behavior is tuned to the characteristic features of the song, such as the carrier frequency and the temporal pattern of sound pulses. Data from behavioral experiments and from neural recordings at different stages of processing in the auditory pathway lead to a concept of serially arranged filtering mechanisms. These encompass a filter for the carrier frequency at the level of the hearing organ, and the pulse duration through phasic onset responses of afferents and reciprocal inhibition of thoracic interneurons. Further, processing by a delay line and coincidence detector circuit in the brain leads to feature detecting neurons that specifically respond to the species-specific pulse rate, and match the characteristics of the phonotactic response. This same circuit may also control the response to the species-specific chirp pattern. Based on these serial filters and the feature detecting mechanism, female phonotactic behavior is shaped and tuned to the characteristic properties of male calling song.Supported by the Biotechnology and Biological Sciences Research Council (BB/J01835X/1) and the Isaac Newton Trust (Trinity College, Cambridge).This is the final version of the article. It first appeared from Frontiers via http://dx.doi.org/10.3389/fphys.2016.0004

Neurosystems: brain rhythms and cognitive processing

Neuronal rhythms are ubiquitous features of brain dynamics, and are highly correlated with cognitive processing. However, the relationship between the physiological mechanisms producing these rhythms and the functions associated with the rhythms remains mysterious. This article investigates the contributions of rhythms to basic cognitive computations (such as filtering signals by coherence and/or frequency) and to major cognitive functions (such as attention and multi-modal coordination). We offer support to the premise that the physiology underlying brain rhythms plays an essential role in how these rhythms facilitate some cognitive operations.098352 - Wellcome Trust; 5R01NS067199 - NINDS NIH HH

An auditory feature detection circuit for sound pattern recognition.

From human language to birdsong and the chirps of insects, acoustic communication is based on amplitude and frequency modulation of sound signals. Whereas frequency processing starts at the level of the hearing organs, temporal features of the sound amplitude such as rhythms or pulse rates require processing by central auditory neurons. Besides several theoretical concepts, brain circuits that detect temporal features of a sound signal are poorly understood. We focused on acoustically communicating field crickets and show how five neurons in the brain of females form an auditory feature detector circuit for the pulse pattern of the male calling song. The processing is based on a coincidence detector mechanism that selectively responds when a direct neural response and an intrinsically delayed response to the sound pulses coincide. This circuit provides the basis for auditory mate recognition in field crickets and reveals a principal mechanism of sensory processing underlying the perception of temporal patterns.Financial support for the study was provided by the Biotechnology and Biological Sciences Research Council (BB/J01835X/1) and the Isaac Newton Trust (Trinity College, Cambridge).This is the final version of the article. It first appeared from AAAS via http://dx.doi.org/10.1126/sciadv.150032

Regulation of Irregular Neuronal Firing by Autaptic Transmission

The importance of self-feedback autaptic transmission in modulating spike-time irregularity is still poorly understood. By using a biophysical model that incorporates autaptic coupling, we here show that self-innervation of neurons participates in the modulation of irregular neuronal firing, primarily by regulating the occurrence frequency of burst firing. In particular, we find that both excitatory and electrical autapses increase the occurrence of burst firing, thus reducing neuronal firing regularity. In contrast, inhibitory autapses suppress burst firing and therefore tend to improve the regularity of neuronal firing. Importantly, we show that these findings are independent of the firing properties of individual neurons, and as such can be observed for neurons operating in different modes. Our results provide an insightful mechanistic understanding of how different types of autapses shape irregular firing at the single-neuron level, and they highlight the functional importance of autaptic self-innervation in taming and modulating neurodynamics.Comment: 27 pages, 8 figure

The claustrum is a highway not a hub : organizing principles of claustrocortical synaptic transmission

The claustrum (CLA) is a brain nucleus wedged between the cortex and striatum. The behaviors it has been implicated in include consciousness, attention, memory and salience detection; dysfunction of CLA circuits is associated with schizophrenia, epilepsy, parkinsonism and disrupted consciousness. While previous research has focused on the gross anatomy of the CLA, it is the functional communication of the CLA with other brain regions that generates behavioral output. Understanding CLA functional connectivity will bring us closer to understanding how the CLA is involved in different behaviors and how these dysfunctions can be remedied. The anterior cingulate cortex-projecting (CLA-ACC) neuron population was used as a model to investigate claustrocortical synaptic transmission. This thesis proposes that the CLA is organized as a highway for connections between brain regions. Paper I revealed that the CLA is organized as functional modules. Specifically, it showed that CLA-ACC neurons receive multicortical input biased towards frontal & limbic cortices rather than sensory cortices, and that CLA-ACC neurons could be segmented into at least two cortical targeting systems. An insular-claustrum- anterior cingulate cortex circuit, which may be the substrate underpinning the Salience Network, was also identified. These findings support feedforward inhibition as a mechanism of action within the CLA. Paper II extended the concept of topological selectivity in the CLA to the single- cell level. Topological selectivity was previously known to exist at a population level. Characterization of the intrinsic electrophysiological properties of individual CLA-ACC neurons revealed four types of CLA-ACC populations. These CLA- ACC neurons were distributed heterogeneously with one type predominant in the anterior and posterior CLA and a second type prominent in the middle of the CLA. Paper III identified the cell-type and layer-specific cortical targets of the CLA. It showed that CLA-ACC neurons provide excitatory monosynaptic input to all layers of the ACC and that different neuron populations receive CLA input in a layer-dependent fashion. From these data, Paper III derived a scheme of CLA targets within a cortex. The findings from this thesis can be summarized using a transportation analogy. Although commonly described as a hub for cortical inputs and outputs, the CLA is likely organized as a collection of highways. A significantly large input should arrive within a small time-window to generate action potentials and enable downstream signal propagation. This is akin to a toll booth with a high toll fee that must be paid-in-full, without delays, before a vehicle can pass through. Projection neurons directed to the same cortical region may have different cell/layer targets. This is comparable to different vehicles on the same highway ending up in different destinations. The findings in this thesis add to our understanding of CLA functional organization by suggesting that any input received by the CLA must be sufficiently strong in order to overcome FFI and for the signal to be propagated. This implies that only input of ethological relevance is processed. Such a mechanism could underlie CLA action across behaviors. This thesis is divided into 6 chapters. Chapter 1 is a preamble. Chapter 2 encompasses the state-of-the-art in CLA and describes the gaps in knowledge that this thesis aims to fill. Chapter 3 clarifies the aims of this thesis. Chapter 4 provides an overview of the methods used. Chapter 5 presents and discusses the main results. Chapter 6 explores the main conclusions from this work. Manuscripts and publications are appended after

Intense Synaptic Activity Enhances Temporal Resolution in Spinal Motoneurons

In neurons, spike timing is determined by integration of synaptic potentials in delicate concert with intrinsic properties. Although the integration time is functionally crucial, it remains elusive during network activity. While mechanisms of rapid processing are well documented in sensory systems, agility in motor systems has received little attention. Here we analyze how intense synaptic activity affects integration time in spinal motoneurons during functional motor activity and report a 10-fold decrease. As a result, action potentials can only be predicted from the membrane potential within 10 ms of their occurrence and detected for less than 10 ms after their occurrence. Being shorter than the average inter-spike interval, the AHP has little effect on integration time and spike timing, which instead is entirely determined by fluctuations in membrane potential caused by the barrage of inhibitory and excitatory synaptic activity. By shortening the effective integration time, this intense synaptic input may serve to facilitate the generation of rapid changes in movements

Interaction of excitation and inhibition in processing of pure tone and amplitude-modulated stimuli in the medial superior olive of the mustached bat

1. In mammals with good low-frequency hearing, the medial superior olive (MSO) processes interaural time or phase differences that are important cues for sound localization. Its cells receive excitatory projections from both cochlear nuclei and are thought to function as coincidence detectors. The response patterns of MSO neurons in most mammals are predominantly sustained. In contrast, the MSO in the mustached bat is a monaural nucleus containing neurons with phasic discharge patterns. These neurons receive projections from the contralateral anteroventral cochlear nucleus (AVCN) and the ipsilateral medial nucleus of the trapezoid body (MNTB). 2. To further investigate the role of the MSO in the bat, the responses of 252 single units in the MSO to pure tones and sinusoidal amplitude-modulated (SAM) stimuli were recorded. The results confirmed that the MSO in the mustached bat is tonotopically organized, with low frequencies in the dorsal part and high frequencies in the ventral part. The 61-kHz region is overrepresented. Most neurons tested (88%) were monaural and discharged only in response to contralateral stimuli. Their response could not be influenced by stimulation of the ipsilateral ear. 3. Only 11% of all MSO neurons were spontaneously active. In these neurons the spontaneous discharge rate was suppressed during the stimulus presentation. 4. The majority of cells (85%) responded with a phasic discharge pattern. About one-half (51%) responded with a level-independent phasic ON response. Other phasic response patterns included phasic OFF or phasic ON-OFF, depending on the stimulus frequency. Neurons with ON-OFF discharge patterns were most common in the 61-kHz region and absent in the high-frequency region. 5. Double tone experiments showed that at short intertone intervals the ON response to the second stimulus or the OFF response to the first stimulus was inhibited. 6. In neuropharmacological experiments, glycine applied to MSO neurons (n = 71) inhibited any tone-evoked response. In the presence of the glycine antagonist strychnine the response patterns changed from phasic to sustained (n = 35) and the neurons responded to both tones presented in double tone experiments independent of the intertone interval (n = 5). The effects of strychnine were reversible. 7. Twenty of 21 neurons tested with sinusoidally amplitude-modulated (SAM) signals exhibited low-pass or band-pass filter characteristics. Tests with SAM signals also revealed a weak temporal summation of inhibition in 13 of the 21 cells tested.(ABSTRACT TRUNCATED AT 400 WORDS) </jats:p

Nanodiamonds-induced effects on neuronal firing of mouse hippocampal microcircuits

Fluorescent nanodiamonds (FND) are carbon-based nanomaterials that can efficiently incorporate optically active photoluminescent centers such as the nitrogen-vacancy complex, thus making them promising candidates as optical biolabels and drug-delivery agents. FNDs exhibit bright fluorescence without photobleaching combined with high uptake rate and low cytotoxicity. Focusing on FNDs interference with neuronal function, here we examined their effect on cultured hippocampal neurons, monitoring the whole network development as well as the electrophysiological properties of single neurons. We observed that FNDs drastically decreased the frequency of inhibitory (from 1.81 Hz to 0.86 Hz) and excitatory (from 1.61 Hz to 0.68 Hz) miniature postsynaptic currents, and consistently reduced action potential (AP) firing frequency (by 36%), as measured by microelectrode arrays. On the contrary, bursts synchronization was preserved, as well as the amplitude of spontaneous inhibitory and excitatory events. Current-clamp recordings revealed that the ratio of neurons responding with AP trains of high-frequency (fast-spiking) versus neurons responding with trains of low-frequency (slow-spiking) was unaltered, suggesting that FNDs exerted a comparable action on neuronal subpopulations. At the single cell level, rapid onset of the somatic AP ("kink") was drastically reduced in FND-treated neurons, suggesting a reduced contribution of axonal and dendritic components while preserving neuronal excitability.Comment: 34 pages, 9 figure

Inhibition Controls Asynchronous States of Neuronal Networks

Computations in cortical circuits require action potentials from excitatory and inhibitory neurons. In this mini-review, I first provide a quick overview of findings that indicate that GABAergic neurons play a fundamental role in coordinating spikes and generating synchronized network activity. Next, I argue that these observations helped popularize the notion that network oscillations require a high degree of spike correlations among interneurons which, in turn, produce synchronous inhibition of the local microcircuit. The aim of this text is to discuss some recent experimental and computational findings that support a complementary view: one in which interneurons participate actively in producing asynchronous states in cortical networks. This requires a proper mixture of shared excitation and inhibition leading to asynchronous activity between neighboring cells. Such contribution from interneurons would be extremely important because it would tend to reduce the spike correlation between neighboring pyramidal cells, a drop in redundancy that could enhance the information-processing capacity of neural networks