Cortical neurons receive synaptic inputs from thousands of afferents that fire action potentials at rates ranging from less than 1 hertz to more than 200 hertz. Both the number of afferents and their large dynamic range can mask changes in the spatial and temporal pattern of synaptic activity, limiting the ability of a cortical neuron to respond to its inputs. Modeling work based on experimental measurements indicates that short-term depression of intracortical synapses provides a dynamic gain-control mechanism that allows equal percentage rate changes on rapidly and slowly firing afferents to produce equal postsynaptic responses. Unlike inhibitory and adaptive mechanisms that reduce responsiveness to all inputs, synaptic depression is input-specific, leading to a dramatic increase in the sensitivity of a neuron to subtle changes in the firing patterns of its afferents.
Cortical synapses exhibit several forms of short-term plasticity, but the contribution of this plasticity to visual response dynamics is unknown. In part, this is because the simple patterns of stimulation used to probe plasticity in vitro do not correspond to patterns of activity that occur in vivo. We have developed a method of quantitatively characterizing short-term plasticity at cortical synapses that permits prediction of responses to arbitrary patterns of stimulation. Synaptic responses were recorded intracellularly as EPSCs and extracellularly as local field potentials in layer 2/3 of rat primary visual cortical slices during stimulation of layer 4 with trains of electrical stimuli containing random mixtures of frequencies. Responses exhibited complex dynamics that were well described by a simple threecomponent model consisting of facilitation and two forms of depression, a stronger form that decayed exponentially with a time constant of several hundred milliseconds and a weaker, but more persistent, form that decayed with a time constant of several seconds. Parameters obtained from fits to one train were used to predict accurately responses to other random and constant frequency trains. Control experiments revealed that depression was not caused by a decrease in the effectiveness of extracellular stimulation or by a buildup of inhibition. Pharmacological manipulations of transmitter release and postsynaptic sensitivity suggested that both forms of depression are mediated presynaptically. These results indicate that firing evoked by visual stimuli is likely to cause significant depression at cortical synapses. Hence synaptic depression may be an important determinant of the temporal features of visual cortical responses.
The stimulus-response function of many visual and auditory neurons has been described by a spatial-temporal receptive field (STRF), a linear model that for mathematical reasons has until recently been estimated with the reverse correlation method, using simple stimulus ensembles such as white noise. Such stimuli, however, often do not effectively activate high-level sensory neurons, which may be optimized to analyze natural sounds and images. We show that it is possible to overcome the simple-stimulus limitation and then use this approach to calculate the STRFs of avian auditory forebrain neurons from an ensemble of birdsongs. We find that in many cases the STRFs derived using natural sounds are strikingly different from the STRFs that we obtained using an ensemble of random tone pips. When we compare these two models by assessing their predictions of neural response to the actual data, we find that the STRFs obtained from natural sounds are superior. Our results show that the STRF model is an incomplete description of response properties of nonlinear auditory neurons, but that linear receptive fields are still useful models for understanding higher level sensory processing, as long as the STRFs are estimated from the responses to relevant complex stimuli.
Sen, Kamal, Frédéric E. Theunissen, and Allison J. Doupe. Feature analysis of natural sounds in the songbird auditory forebrain. J Neurophysiol 86: 1445Neurophysiol 86: -1458Neurophysiol 86: , 2001. Although understanding the processing of natural sounds is an important goal in auditory neuroscience, relatively little is known about the neural coding of these sounds. Recently we demonstrated that the spectral temporal receptive field (STRF), a description of the stimulus-response function of auditory neurons, could be derived from responses to arbitrary ensembles of complex sounds including vocalizations. In this study, we use this method to investigate the auditory processing of natural sounds in the birdsong system. We obtain neural responses from several regions of the songbird auditory forebrain to a large ensemble of bird songs and use these data to calculate the STRFs, which are the best linear model of the spectral-temporal features of sound to which auditory neurons respond. We find that these neurons respond to a wide variety of features in songs ranging from simple tonal components to more complex spectral-temporal structures such as frequency sweeps and multi-peaked frequency stacks. We quantify spectral and temporal characteristics of these features by extracting several parameters from the STRFs. Moreover, we assess the linearity versus nonlinearity of encoding by quantifying the quality of the predictions of the neural responses to songs obtained using the STRFs. Our results reveal successively complex functional stages of song analysis by neurons in the auditory forebrain. When we map the properties of auditory forebrain neurons, as characterized by the STRF parameters, onto conventional anatomical subdivisions of the auditory forebrain, we find that although some properties are shared across different subregions, the distribution of several parameters is suggestive of hierarchical processing.
Narayan, Rajiv, Gilberto Grañ a, and Kamal Sen. Distinct time scales in cortical discrimination of natural sounds in songbirds. J Neurophysiol 96: 252-258, 2006; doi:10.1152/jn.01257.2005. Understanding how single cortical neurons discriminate between sensory stimuli is fundamental to providing a link between cortical neural responses and perception. The discrimination of sensory stimuli by cortical neurons has been intensively investigated in the visual and somatosensory systems. However, relatively little is known about discrimination of sounds by auditory cortical neurons. Auditory cortex plays a particularly important role in the discrimination of complex sounds, e.g., vocal communication sounds. The rich dynamic structure of such complex sounds on multiple time scales motivates two questions regarding cortical discrimination. How does discrimination depend on the temporal resolution of the cortical response? How does discrimination accuracy evolve over time? Here we investigate these questions in field L, the analogue of primary auditory cortex in zebra finches, analyzing temporal resolution and temporal integration in the discrimination of conspecific songs (songs of the bird's own species) for both anesthetized and awake subjects. We demonstrate the existence of distinct time scales for temporal resolution and temporal integration and explain how they arise from cortical neural responses to complex dynamic sounds.
A central finding in many cortical areas is that single neurons can match behavioral performance in the discrimination of sensory stimuli. However, whether this is true for natural behaviors involving complex natural stimuli remains unknown. Here we use the model system of songbirds to address this problem. Specifically, we investigate whether neurons in field L, the homolog of primary auditory cortex, can match behavioral performance in the discrimination of conspecific songs. We use a classification framework based on the (dis)similarity between single spike trains to quantify neural discrimination. We use this framework to investigate the discriminability of single spike trains in field L in response to conspecific songs, testing different candidate neural codes underlying discrimination. We find that performance based on spike timing is significantly higher than performance based on spike rate and interspike intervals. We then assess the impact of temporal correlations in spike trains on discrimination. In contrast to widely discussed effects of correlations in limiting the accuracy of a population code, temporal correlations appear to improve the performance of single neurons in the majority of cases. Finally, we compare neural performance with behavioral performance. We find a diverse range of performance levels in field L, with neural performance matching behavioral accuracy only for the best neurons using a spike-timing-based code.
At least 10 different substances modulate the amplitude of nerve-evoked contractions of the gastric mill 4 (gm4) muscle of the crab, Cancer borealis. Serotonin, dopamine, octopamine, proctolin, red pigment concentrating hormone, crustacean cardioactive peptide, TNRNFLRFamide, and SDRNFLRFamide increased and -allatostatin-3 and histamine decreased the amplitude of nerve-evoked contractions. Modulator efficacy was frequency dependent; TNRNFLRFamide, proctolin, and allatostatin-3 were more effective when the motor neuron was stimulated at 10 Hz than at 40 Hz, whereas the reverse was true for dopamine and serotonin. The modulators that were most effective at high stimulus frequencies produced a significant decrease in muscle relaxation time; those that were most effective at low stimulus frequencies produced modest increases in relaxation time. Thus modulator actions that appear redundant when examined only at one stimulus frequency are differentiated when a range of stimulus dynamics is studied. The effects of TNRNFLRFamide, serotonin, proctolin, dopamine, and -allatostatin-3 on the amplitude and facilitation of nerve-evoked excitatory junctional potentials (EJPs) in the gm4 and gastric mill 6 (gm6) muscles were compared. The EJPs in gm4 have a large initial amplitude and show relatively little facilitation, whereas the EJPs in gm6 have a small initial amplitude and show considerable facilitation. Modulators that enhanced contractions also enhanced EJP amplitude; -allatostatin-3 reduced EJP amplitude. The effects of these modulators on EJP amplitude were modest and showed no significant frequency dependence. This suggests that the frequency dependence of modulator action on contraction results from effects on excitation-contraction coupling. The modulators affected facilitation at these junctions in a manner consistent with a change in release probability. They produced a change in facilitation that is inversely related to their action on EJP amplitude.
Humans and animals must often discriminate between complex natural sounds in the presence of competing sounds (maskers). Although the auditory cortex is thought to be important in this task, the impact of maskers on cortical discrimination remains poorly understood. We examined neural responses in zebra finch (Taeniopygia guttata) field L (homologous to primary auditory cortex) to target birdsongs that were embedded in three different maskers (broadband noise, modulated noise and birdsong chorus). We found two distinct forms of interference in the neural responses: the addition of spurious spikes occurring primarily during the silent gaps between song syllables and the suppression of informative spikes occurring primarily during the syllables. Both effects systematically degraded neural discrimination as the target intensity decreased relative to that of the masker. The behavioral performance of songbirds degraded in a parallel manner. Our results identify neural interference that could explain the perceptual interference at the heart of the cocktail party problem.
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