Article

Nelken, I. Processing of complex stimuli and natural scenes in the auditory cortex. Curr. Opin. Neurobiol. 14, 474-480

Department of Neurobiology, The Silberman Institute of Life Sciences, and the Interdisciplinary Center for Neural Computations, Givat Ram 91904, Jerusalem, Israel.
Current Opinion in Neurobiology (Impact Factor: 6.63). 09/2004; 14(4):474-80. DOI: 10.1016/j.conb.2004.06.005
Source: PubMed

ABSTRACT

Neuronal responses in auditory cortex show a fascinating mixture of characteristics that span the range from almost perfect copies of physical aspects of the stimuli to extremely complex context-dependent responses. Fast, highly stimulus-specific adaptation and slower plastic mechanisms work together to constantly adjust neuronal response properties to the statistics of the auditory scene. Evidence with converging implications suggests that the neuronal activity in primary auditory cortex represents sounds in terms of auditory objects rather than in terms of invariant acoustic features.

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    • "In the fields of vision and audition, the receptive fields of central neurons are tuned to the statistics of the 'natural scene', that is, the stimuli that the animal is likely to encounter in its natural environment. Thus, neurons of primary visual cortex are tuned for the horizontal orientations and low spatial frequencies that dominate natural scenes (Vinje and Gallant, 2000; David et al., 2004), whereas neurons of higher-level auditory centers select for the sounds of the animal's vocalizations in terms of auditory objects rather than invariant acoustic features (Margoliash, 1983, 1986; Rauschecker et al., 1995; Ohlemiller et al., 1996; Nelken, 2004). Analysis of natural scene statistics has proven to be a powerful approach for understanding neural coding within audition and vision, but has yet to be generally applied to the somatosensory system, although some work has been done on texture (Ritt et al., 2008; Manfredi et al., 2014). "
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    ABSTRACT: Analysis of natural scene statistics has been a powerful approach for understanding neural coding in the auditory and visual systems. In the field of somatosensation, it has been more challenging to quantify the natural tactile scene, in part because somatosensory signals are so tightly linked to the animal's movements. The present work takes a step towards quantifying the natural tactile scene for the rat vibrissal system by simulating rat whisking motions to systematically investigate the probabilities of whisker-object contact in naturalistic environments. The simulations permit an exhaustive search through the complete space of possible contact patterns, thereby allowing for the characterization of the patterns that would most likely occur during long sequences of natural exploratory behavior. We specifically quantified the probabilities of 'concomitant contact', that is, given that a particular whisker makes contact with a surface during a whisk, what is the probability that each of the other whiskers will also make contact with the surface during that whisk? Probabilities of concomitant contact were quantified in simulations that assumed increasingly naturalistic conditions: first, the space of all possible head poses; second, the space of behaviorally preferred head poses as measured experimentally; and third, common head poses in environments such as cages and burrows. As environments became more naturalistic, the probability distributions shifted from exhibiting a 'row-wise' structure to a more diagonal structure. Results also reveal that the rat appears to use motor strategies (e.g. head pitches) that generate contact patterns that are particularly well suited to extract information in the presence of uncertainty. © 2015. Published by The Company of Biologists Ltd.
    Preview · Article · Aug 2015 · Journal of Experimental Biology
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    • "In other words, the neuron's previous experience determines its future sensitivity, which suggests SSA may be a basic mechanism underlying predictive coding (Friston, 2005; Baldeweg, 2006; Bar, 2007; Winkler et al., 2009; Bendixen et al., 2012). Moreover, previous studies have also suggested that SSA could be linked to auditory memory, recognition of acoustic objects and auditory scene analysis (Nelken, 2004; Winkler et al., 2009). "
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    ABSTRACT: To follow an ever-changing auditory scene, the auditory brain is continuously creating a representation of the past to form expectations about the future. Unexpected events will produce an error in the predictions that should "trigger" the network's response. Indeed, neurons in the auditory midbrain, thalamus and cortex, respond to rarely occurring sounds while adapting to frequently repeated ones, i.e., they exhibit stimulus specific adaptation (SSA). SSA cannot be explained solely by intrinsic membrane properties, but likely involves the participation of the network. Thus, SSA is envisaged as a high order form of adaptation that requires the influence of cortical areas. However, present research supports the hypothesis that SSA, at least in its simplest form (i.e., to frequency deviants), can be transmitted in a bottom-up manner through the auditory pathway. Here, we briefly review the underlying neuroanatomy of the corticofugal projections before discussing state of the art studies which demonstrate that SSA present in the medial geniculate body (MGB) and inferior colliculus (IC) is not inherited from the cortex but can be modulated by the cortex via the corticofugal pathways. By modulating the gain of neurons in the thalamus and midbrain, the auditory cortex (AC) would refine SSA subcortically, preventing irrelevant information from reaching the cortex.
    Full-text · Article · Mar 2015 · Frontiers in Systems Neuroscience
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    • "In contrast to the above view and in concordance with previous computational studies (Buonomano & Merzenich, 1995; May & Tiitinen , 2007, 2010; Buonomano & Maass, 2009), the current results demonstrate that synaptic adaptation might have an unexpected function in contributing to temporal integration of auditory information – possibly the central function of auditory cortex (Nelken, 2004) – by allowing for individual cortical neurons to respond selectively to the temporal structure of stimuli. A counterintuitive consequence of this is that activity-dependent depression of excitatory synapses between pyramidal cell populations not only leads to forward suppression in the case of masker–tone interactions, but could also underlie response facilitation reflecting temporal selectivity (see also Goudar & Buonomano, 2014). "
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    ABSTRACT: Incoming sounds are represented in the context of preceding events, and this requires a memory mechanism that integrates information over time. Here, it was demonstrated that response adaptation, the suppression of neural responses due to stimulus repetition, might reflect a computational solution that auditory cortex uses for temporal integration. Adaptation is observed in single-unit measurements as two-tone forward masking effects and as stimulus-specific adaptation (SSA). In non-invasive observations, the amplitude of the auditory N1m response adapts strongly with stimulus repetition, and it is followed by response recovery (the so-called mismatch response) to rare deviant events. The current computational simulations described the serial core-belt-parabelt structure of auditory cortex, and included synaptic adaptation, the short-term, activity-dependent depression of excitatory corticocortical connections. It was found that synaptic adaptation is sufficient for columns to respond selectively to tone pairs and complex tone sequences. These responses were defined as combination sensitive, thus reflecting temporal integration, when a strong response to a stimulus sequence was coupled with weaker responses both to the time-reversed sequence and to the isolated sequence elements. The temporal complexity of the stimulus seemed to be reflected in the proportion of combination-sensitive columns across the different regions of the model. Our results suggest that while synaptic adaptation produces facilitation and suppression effects, including SSA and the modulation of the N1m response, its functional significance may actually be in its contribution to temporal integration. This integration seems to benefit from the serial structure of auditory cortex. © 2015 Federation of European Neuroscience Societies and John Wiley & Sons Ltd.
    Full-text · Article · Mar 2015 · European Journal of Neuroscience
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