- Email: [email protected]
Sensory systems
Sensory systems Editorial Overview Catherine Dulac and Benedikt Grothe Current Opinion in Neurobiology 2004, 14:403–406 Available online 20th July 2004 0959-4388/$ – see front matter ß 2004 Elsevier Ltd. All rights reserved. DOI 10.1016/j.conb.2004.07.010
Catherine Dulac Professor of Molecular and Cellular Biology, Howard Hughes Medical Institute, Department of Molecular and Cellular Biology, Harvard University, 16 Divinity Avenue, Cambridge, 02138 MA, USA e-mail: [email protected]
Our research group is interested in the molecular logic of pheromone detection leading to behavioral changes in mammals, and in the analysis of olfactory development. Benedikt Grothe Research Group Auditory Processing, Max Planck Institute of Neurobiology, Am Klopferspitz 18a, 82152 Martinsried, Germany e-mail: [email protected]
Benedikt Grothe and his group are interested in the cellular and network properties of time analyzing neurons and neuronal circuits in the mammalian auditory brainstem. In particular, they study the role of neural inhibition in temporal processing, its evolution, and its ontogeny with special focus on the role of early sensory experience in tuning single neurons to temporal cues of particular behavioral relevance.
www.sciencedirect.com
Introduction The field of sensory neurobiology is old — one of the oldest in the neurosciences. And luckily it has retained some of its old charm that stems from the comparative approach and the use of a wide range of animal models — sometimes as weird as naked mole rats, jelly fish or spiders, all animals that will be represented in the various reviews of this issue. At the same time, the work on sensory systems is as vibrant as ever. This is partially because of the dramatically increasing number of insights into the molecular basis of sensory transduction mechanisms and the accelerating technical progress allowing new approaches for analyzing complex neuronal responses at high levels of sensory information processing. However, to a large degree the exciting news comes from new concepts, some of which have only been developed in the past few years. This is most obvious in the field of processing by higher order neurons, where a significant shift in stimulus paradigms now leads to new insights of how sensory systems analyze natural stimuli in a natural environment.
Evolution of sensory systems The common or divergent evolutionary origin of specific organs, including sensory organs and corresponding brain areas, is a central issue for the understanding of animal evolution and evolution of behavior. In agreement with evolutionary principles and mechanisms uniting all fields of biology, this issue of Current Opinion in Neurobiology, which deals with sensory systems, also starts with the question of homology of sensory systems across different clades of animals. In his review, Nilsson addresses the question of the evolutionary origin of complex eyes. Although it is unclear from the fossil record whether or not early vertebrates had eyes, the current belief is that there was a common origin of all eyes during the Cambrian explosion, some 560 million years ago, and hence, that eyes in recent bilateral animals (and the vast majority of animals belong to Bilateria) share a common ancestor. This concept is mainly formed on the basis of molecular and functional identification of orthologs of the transcription factor Pax6 in distinct animal phyla. During the past decade the dominant view proposed that because Pax 6 functions as a master regulator of eye development in various vertebrate and invertebrate species, eyes as different as insect compound eyes and vertebrate lens eyes must be evolutionary homologs. Nilsson in his review, however, carefully discriminates between the developmental regulatory circuit of photoreception and the molecular and cellular mechanisms of vision, and at the same time emphasizes the important distinction between rhabdomeric and ciliary photoreceptors. This leads to a much more differentiated view, which is more in line with older views of parallel evolution of complex eyes. In his conclusion, Nilsson highlights the major role in eye Current Opinion in Neurobiology 2004, 14:403–406
404 Sensory systems
evolution of new insight coming from studies dealing with non-bilateral animals: Cnidaria. Thus, even in times of clear dominance of a small number of animal models, comparative approaches and the use of exotic model animals, such as jellyfish, spiders, scorpions or naked mole rats (see also reviews by Barth or Lewin et al.) do retain enormous significance. On the one hand, comparative approaches are compulsory to understand the evolution of sensory systems and to appreciate how different animal groups were able to offer different solutions to achieving similar sensory tasks. Interestingly, sometimes it appears that the physical constraints only allow one solution (see the discussion in this issue of the basic design of mechano-receptors in arachnids by Barth). On the other hand, it can be misleading if strategies evolved in one group of animals to deal with a specific physical stimulus parameter are assigned to other groups of animals (see review by Palmer and below).
Molecular and cellular mechanisms of sensory detection: insights from coding to behavior strategies A similar case of apparent parallel (independent) evolution is exemplified by Barth. Recent findings indicate that the transduction mechanism in arachnid slit sensilla, tiny mechanoreceptors that sense tension of the cuticula allowing the detection of minute surface vibrations, differs from most other mechanoreceptor transduction mechanisms (such as, for instance, in inner ear hair cells), in that the receptor current is carried by Na+. The review by Barth also provides profound inside information into the evolutionary and biophysical constraints that lead to the development of a probably unrivaled battery of different mechanoreceptors in arachnids. A fascinating comparison of distinct cellular and molecular strategies evolved by animals to achieve optimal chemosensory detection is provided by three reviews, one devoted to vertebrate taste (Scott), and one to invertebrate (Amrein), and one to vertebrate pheromone detection (Luo and Katz). The review by Scott enlightens the reader as to how the recent molecular and functional identification of distinct receptor families and signaling pathways mediating sweet, bitter, and amino acid taste detection in mammals have provided a novel understanding of mammalian taste coding. It appears that, by virtue of expression of specific receptor genes or combinations of genes, individual taste cells are tuned to a specific taste modality. Expression of two receptors T1R1+3 provides wide sensitivity to amino acids, a sensory modality encompassing the sense of umami (monosodium glutamate) in humans, whereas expression of T1R2+3 generates a broadly tuned sweet receptor. By contrast, broad tuning to bitter compounds by individual taste cells results from the expression of Current Opinion in Neurobiology 2004, 14:403–406
multiple T2Rs in a single cell, with each individual receptor narrowly tuned to a few bitter substances. These data suggest, therefore, a ‘labeled line’ model of taste coding, according to which the specificity of taste perception results from stimulation of distinct subsets of taste cells. Interestingly, Luo and Katz also introduce the idea of a labeled line code in pheromone detection in their review, and emphasize the similarities and differences with the principles of chemosensory coding used in olfaction and taste. Luo and Katz describe how, in contrast to taste, but similarly to olfaction, pheromone sensing neurons of the vomeronasal organ (VNO) express only one receptor gene of the V1R or the V2R family. However, in contrast to the current understanding of olfactory detection, vomeronasal detection by single receptor types appears amazingly specific and sensitive, and this concurs with the extreme specificity of mitral cell stimulation in the accessory olfactory bulb. The complexity of the VNO neuronal projection to the brain leads to a more difficult interpretation of pheromone sensory coding at this level. It is particularly interesting to contrast these two chemosensory strategies to that used in the fruitfly to detect pheromones. Drosophila, like most animals, adapts various aspects of its courtship behavior in response to chemical cues emitted by conspecifics (Amrein). The expression of pheromone receptor molecules, which in the fly are related to gustatory receptors in sensory antennae but also in peripheral organs such as the legs point to the existence of central as well as peripheral circuits regulating genetically pre-programmed behaviors. As emphasized by Amrein, useful comparison can be made among evolutionarily distant species, providing significant insight into the mechanisms of detection and processing of evolutionarily important and sexually dimorphic signals.
Detection thresholds and the modulation of sensory perception and physiological state Advances in molecular and imaging approaches have led to increasingly comprehensive investigations of the modulation of perceptual and behavioral output triggered by sensory stimuli. As emphasized by Lewin et al., the perception of pain is highly variable according to physiological or pathological state. In turn, the modulation of pain sensation, a central issue for the understanding and treatment of chronic pain, appears to be a complex and multi-layered phenomenon resulting from peripheral as well as central sensitization. The discovery of distantly related members of the transient receptor potential (TRP) family of ion channels involved in thermal and inflammatory nociception, as well as other key players of the nociceptive signal transduction pathway, have led to new insights into both www.sciencedirect.com
Editorial overview Dulac and Grothe 405
normal somatosensory detection and changes occurring during hyperalgesia and allodynia. In turn, the study of central sensitization has revealed the usual suspects of central plasticity, including N-methyl-D-aspartate (NMDA) and non-NMDA glutamate receptors. These very same mechanisms also come to play in studies of sensory processing performed at a different level, that of the entire organism, Caenorhabditis elegans. Whittaker and Sternberg walk us through the coordination of motor programs in C. elegans as triggered and modulated by external sensory stimuli and internal physiological states.
More on sensory coding One of the examples for labeled line processing independently of receptor surfaces has been the auditory localization system with computational space maps in the barn owl that had been widely accepted for mammals as well, although without convincing experimental proof. As Palmer discusses in this issue, recent studies provide strong evidence against a labeled line system in the mammalian auditory localization system, particularly for low frequency sounds. Rather, there appears to be a population code established, which is more in line with the notoriously unfruitful attempts to show the widely expected systematic representation of auditory space or even a highly specific sensitivity of single neurons in the mammalian auditory cortex. An interesting link between rather complex sensory processing and a simple feature of the receptor cells, in this case the inner hair cells in the mammalian inner ear and their synapses, is put forward by Heil’s review. He argues that the first spike driven by an auditory stimulus, which carries a larger amount of information than commonly appreciated, is not simply related to a point in time when the stimulus reaches a fixed threshold, but rather to a temporal integration of the amplitude envelope of the sound. This integrative threshold (and thereby the timing) of the first stimulus driven spike could be caused by the presynaptic processes in the synapses between the inner hair cells and the auditory nerve fibers. Based on the time courses known, Heil speculates that this process is governed by the completion of the calcium-binding steps required for exocytosis. In principle, there is no reason to believe that this is only applicable to the auditory system.
Neural representation of complex stimuli, streaming One of the major advances in sensory neuroscience comes from studies investigating the neuronal principles underlying the analysis of context dependent complex stimuli in higher order neurons. The major progress here comes from the use of natural stimuli and natural scenes, as Kayser et al. point out in their review. Use of simple unnatural stimuli is adequate for scrutinizing the rules underlying the basic analysis of the physical cues inherent in each sensory stimulus. In fact, mapping neurons using www.sciencedirect.com
reverse correlation to assess sensory receptive fields of single neurons or ensembles of neurons (spatio-temporal receptive fields, STRFS) became the dominating tool in vision, as in audition. Although this method adds quite significantly to our understanding of sensory processing in the lower and medial stations of the processing hierarchy, it basically fails to explain the responses of higher order neurons in the visual system, similar to the way that detection of orientation context in V1 can sometimes lead to misleading interpretations. In their review, Kayser et al. convincingly point out that the visual system did not evolve to process simple stimuli but to analyze complex scenes. Accordingly, responses to natural, hence, complex stimuli, are often different from what can predicted from responses to simple stimuli. As Nelken states in his review, the field of auditory research is somewhat behind when it comes to the neural basis of natural scene analysis. This, however, could be partially excused by the unrivaled complexity of subcortical auditory processing and the extraordinary importance of temporal cues in audition. Nevertheless, as Kayser et al. argue for the visual system, Nelken describes for the auditory system how traditional approaches also lead to some misconceptions, due to the use of unnatural stimuli. Importantly, Nelken provides a working hypothesis for a hierarchical system of auditory processing stating that feature extraction is already achieved in the auditory system at pre-cortical levels — potentially a fundamental difference to the visual system — and auditory object formation is the main task of the primary auditory cortex. This is in line with increasing evidence for a complex context sensitivity in the auditory cortex, comparable only to that found in secondary cortical areas in the visual system (such as V1). To conclude this section of the issue, Olshausen and Field comment on the topic of sparse coding, the idea that only a few higher order sensory neurons represent relevant sensory information at any given point in time. This is again related to the question of context dependent processing of behaviorally relevant natural stimuli at higher stages of sensory processing. Although the concept of sparse coding is not new, there is increasing experimental evidence supporting it.
Context dependency, behavioral state and more Context dependent responses are not a sole characteristic of cortical areas. This is not a novel concept, but the review by Hurley et al. summarizes the dramatic success that has occurred in the field of neuromodulation. Focusing on serotonin and norepinephrine, they summarize some of the most important effects of neuromodulators on feature extraction neurons as well as on higher functions. In general, these effects are complex and go far beyond simple gain control functions, for instance, they differentially modulate specific properties of receptive fields. Thereby, they can alter the entire representation of a stimulus Current Opinion in Neurobiology 2004, 14:403–406
406 Sensory systems
feature in large populations of neurons, which can be directly related to the attentional state of an animal. A specific example of the effect of neuromodulators is discussed in the review by Prather and Mooney, who discuss recent progress in understanding the functional interplay among the different forebrain nuclei in the bird song system, in particular, in the context of recognition of conspecific songs. One of these nuclei, HVC and its inherent microcircuit, appears to be selectively reconfigured by the action of cholinergic and other neuromodulatory inputs, which depend on the bird’s behavioral state. Furthermore, the authors demonstrate the unrivaled conceptual beauty of the bird song system when it comes to understanding the interplay of learning, recognition, and resulting motor action and their neural substrates.
Influence of experience on sensory development and processing Pioneering experiments in the retina have revealed the influence of stimulation early in development of
Current Opinion in Neurobiology 2004, 14:403–406
peripheral organs on the development and maturation of sensory pathways. Grubb and Thompson review the large diversity of mechanisms by which the external environment, through early, and sometimes very early sensory activity and spontaneous activity, ensures appropriate maturation of sensory circuits. In addition to its mark on sensory pathway development, sensory experience also alters mature circuits, thus providing a basis for perceptual learning. In his review, Ghose provides an update on recent psychological and physiological studies addressing the variety of cortical processing strategies aimed at improving perceptual capabilities. Taken together, the current issue provides a cross section through recent advances in most sensory systems covering the broad range of levels in sensory processing from molecules up to perception. Nevertheless, we hope that it becomes apparent that there are some dominating themes crossing the bridges from one sense to others, as for instance in natural scene analysis.
www.sciencedirect.com
Catherine Dulac Professor of Molecular and Cellular Biology, Howard Hughes Medical Institute, Department of Molecular and Cellular Biology, Harvard University, 16 Divinity Avenue, Cambridge, 02138 MA, USA e-mail: [email protected]
Our research group is interested in the molecular logic of pheromone detection leading to behavioral changes in mammals, and in the analysis of olfactory development. Benedikt Grothe Research Group Auditory Processing, Max Planck Institute of Neurobiology, Am Klopferspitz 18a, 82152 Martinsried, Germany e-mail: [email protected]
Benedikt Grothe and his group are interested in the cellular and network properties of time analyzing neurons and neuronal circuits in the mammalian auditory brainstem. In particular, they study the role of neural inhibition in temporal processing, its evolution, and its ontogeny with special focus on the role of early sensory experience in tuning single neurons to temporal cues of particular behavioral relevance.
www.sciencedirect.com
Introduction The field of sensory neurobiology is old — one of the oldest in the neurosciences. And luckily it has retained some of its old charm that stems from the comparative approach and the use of a wide range of animal models — sometimes as weird as naked mole rats, jelly fish or spiders, all animals that will be represented in the various reviews of this issue. At the same time, the work on sensory systems is as vibrant as ever. This is partially because of the dramatically increasing number of insights into the molecular basis of sensory transduction mechanisms and the accelerating technical progress allowing new approaches for analyzing complex neuronal responses at high levels of sensory information processing. However, to a large degree the exciting news comes from new concepts, some of which have only been developed in the past few years. This is most obvious in the field of processing by higher order neurons, where a significant shift in stimulus paradigms now leads to new insights of how sensory systems analyze natural stimuli in a natural environment.
Evolution of sensory systems The common or divergent evolutionary origin of specific organs, including sensory organs and corresponding brain areas, is a central issue for the understanding of animal evolution and evolution of behavior. In agreement with evolutionary principles and mechanisms uniting all fields of biology, this issue of Current Opinion in Neurobiology, which deals with sensory systems, also starts with the question of homology of sensory systems across different clades of animals. In his review, Nilsson addresses the question of the evolutionary origin of complex eyes. Although it is unclear from the fossil record whether or not early vertebrates had eyes, the current belief is that there was a common origin of all eyes during the Cambrian explosion, some 560 million years ago, and hence, that eyes in recent bilateral animals (and the vast majority of animals belong to Bilateria) share a common ancestor. This concept is mainly formed on the basis of molecular and functional identification of orthologs of the transcription factor Pax6 in distinct animal phyla. During the past decade the dominant view proposed that because Pax 6 functions as a master regulator of eye development in various vertebrate and invertebrate species, eyes as different as insect compound eyes and vertebrate lens eyes must be evolutionary homologs. Nilsson in his review, however, carefully discriminates between the developmental regulatory circuit of photoreception and the molecular and cellular mechanisms of vision, and at the same time emphasizes the important distinction between rhabdomeric and ciliary photoreceptors. This leads to a much more differentiated view, which is more in line with older views of parallel evolution of complex eyes. In his conclusion, Nilsson highlights the major role in eye Current Opinion in Neurobiology 2004, 14:403–406
404 Sensory systems
evolution of new insight coming from studies dealing with non-bilateral animals: Cnidaria. Thus, even in times of clear dominance of a small number of animal models, comparative approaches and the use of exotic model animals, such as jellyfish, spiders, scorpions or naked mole rats (see also reviews by Barth or Lewin et al.) do retain enormous significance. On the one hand, comparative approaches are compulsory to understand the evolution of sensory systems and to appreciate how different animal groups were able to offer different solutions to achieving similar sensory tasks. Interestingly, sometimes it appears that the physical constraints only allow one solution (see the discussion in this issue of the basic design of mechano-receptors in arachnids by Barth). On the other hand, it can be misleading if strategies evolved in one group of animals to deal with a specific physical stimulus parameter are assigned to other groups of animals (see review by Palmer and below).
Molecular and cellular mechanisms of sensory detection: insights from coding to behavior strategies A similar case of apparent parallel (independent) evolution is exemplified by Barth. Recent findings indicate that the transduction mechanism in arachnid slit sensilla, tiny mechanoreceptors that sense tension of the cuticula allowing the detection of minute surface vibrations, differs from most other mechanoreceptor transduction mechanisms (such as, for instance, in inner ear hair cells), in that the receptor current is carried by Na+. The review by Barth also provides profound inside information into the evolutionary and biophysical constraints that lead to the development of a probably unrivaled battery of different mechanoreceptors in arachnids. A fascinating comparison of distinct cellular and molecular strategies evolved by animals to achieve optimal chemosensory detection is provided by three reviews, one devoted to vertebrate taste (Scott), and one to invertebrate (Amrein), and one to vertebrate pheromone detection (Luo and Katz). The review by Scott enlightens the reader as to how the recent molecular and functional identification of distinct receptor families and signaling pathways mediating sweet, bitter, and amino acid taste detection in mammals have provided a novel understanding of mammalian taste coding. It appears that, by virtue of expression of specific receptor genes or combinations of genes, individual taste cells are tuned to a specific taste modality. Expression of two receptors T1R1+3 provides wide sensitivity to amino acids, a sensory modality encompassing the sense of umami (monosodium glutamate) in humans, whereas expression of T1R2+3 generates a broadly tuned sweet receptor. By contrast, broad tuning to bitter compounds by individual taste cells results from the expression of Current Opinion in Neurobiology 2004, 14:403–406
multiple T2Rs in a single cell, with each individual receptor narrowly tuned to a few bitter substances. These data suggest, therefore, a ‘labeled line’ model of taste coding, according to which the specificity of taste perception results from stimulation of distinct subsets of taste cells. Interestingly, Luo and Katz also introduce the idea of a labeled line code in pheromone detection in their review, and emphasize the similarities and differences with the principles of chemosensory coding used in olfaction and taste. Luo and Katz describe how, in contrast to taste, but similarly to olfaction, pheromone sensing neurons of the vomeronasal organ (VNO) express only one receptor gene of the V1R or the V2R family. However, in contrast to the current understanding of olfactory detection, vomeronasal detection by single receptor types appears amazingly specific and sensitive, and this concurs with the extreme specificity of mitral cell stimulation in the accessory olfactory bulb. The complexity of the VNO neuronal projection to the brain leads to a more difficult interpretation of pheromone sensory coding at this level. It is particularly interesting to contrast these two chemosensory strategies to that used in the fruitfly to detect pheromones. Drosophila, like most animals, adapts various aspects of its courtship behavior in response to chemical cues emitted by conspecifics (Amrein). The expression of pheromone receptor molecules, which in the fly are related to gustatory receptors in sensory antennae but also in peripheral organs such as the legs point to the existence of central as well as peripheral circuits regulating genetically pre-programmed behaviors. As emphasized by Amrein, useful comparison can be made among evolutionarily distant species, providing significant insight into the mechanisms of detection and processing of evolutionarily important and sexually dimorphic signals.
Detection thresholds and the modulation of sensory perception and physiological state Advances in molecular and imaging approaches have led to increasingly comprehensive investigations of the modulation of perceptual and behavioral output triggered by sensory stimuli. As emphasized by Lewin et al., the perception of pain is highly variable according to physiological or pathological state. In turn, the modulation of pain sensation, a central issue for the understanding and treatment of chronic pain, appears to be a complex and multi-layered phenomenon resulting from peripheral as well as central sensitization. The discovery of distantly related members of the transient receptor potential (TRP) family of ion channels involved in thermal and inflammatory nociception, as well as other key players of the nociceptive signal transduction pathway, have led to new insights into both www.sciencedirect.com
Editorial overview Dulac and Grothe 405
normal somatosensory detection and changes occurring during hyperalgesia and allodynia. In turn, the study of central sensitization has revealed the usual suspects of central plasticity, including N-methyl-D-aspartate (NMDA) and non-NMDA glutamate receptors. These very same mechanisms also come to play in studies of sensory processing performed at a different level, that of the entire organism, Caenorhabditis elegans. Whittaker and Sternberg walk us through the coordination of motor programs in C. elegans as triggered and modulated by external sensory stimuli and internal physiological states.
More on sensory coding One of the examples for labeled line processing independently of receptor surfaces has been the auditory localization system with computational space maps in the barn owl that had been widely accepted for mammals as well, although without convincing experimental proof. As Palmer discusses in this issue, recent studies provide strong evidence against a labeled line system in the mammalian auditory localization system, particularly for low frequency sounds. Rather, there appears to be a population code established, which is more in line with the notoriously unfruitful attempts to show the widely expected systematic representation of auditory space or even a highly specific sensitivity of single neurons in the mammalian auditory cortex. An interesting link between rather complex sensory processing and a simple feature of the receptor cells, in this case the inner hair cells in the mammalian inner ear and their synapses, is put forward by Heil’s review. He argues that the first spike driven by an auditory stimulus, which carries a larger amount of information than commonly appreciated, is not simply related to a point in time when the stimulus reaches a fixed threshold, but rather to a temporal integration of the amplitude envelope of the sound. This integrative threshold (and thereby the timing) of the first stimulus driven spike could be caused by the presynaptic processes in the synapses between the inner hair cells and the auditory nerve fibers. Based on the time courses known, Heil speculates that this process is governed by the completion of the calcium-binding steps required for exocytosis. In principle, there is no reason to believe that this is only applicable to the auditory system.
Neural representation of complex stimuli, streaming One of the major advances in sensory neuroscience comes from studies investigating the neuronal principles underlying the analysis of context dependent complex stimuli in higher order neurons. The major progress here comes from the use of natural stimuli and natural scenes, as Kayser et al. point out in their review. Use of simple unnatural stimuli is adequate for scrutinizing the rules underlying the basic analysis of the physical cues inherent in each sensory stimulus. In fact, mapping neurons using www.sciencedirect.com
reverse correlation to assess sensory receptive fields of single neurons or ensembles of neurons (spatio-temporal receptive fields, STRFS) became the dominating tool in vision, as in audition. Although this method adds quite significantly to our understanding of sensory processing in the lower and medial stations of the processing hierarchy, it basically fails to explain the responses of higher order neurons in the visual system, similar to the way that detection of orientation context in V1 can sometimes lead to misleading interpretations. In their review, Kayser et al. convincingly point out that the visual system did not evolve to process simple stimuli but to analyze complex scenes. Accordingly, responses to natural, hence, complex stimuli, are often different from what can predicted from responses to simple stimuli. As Nelken states in his review, the field of auditory research is somewhat behind when it comes to the neural basis of natural scene analysis. This, however, could be partially excused by the unrivaled complexity of subcortical auditory processing and the extraordinary importance of temporal cues in audition. Nevertheless, as Kayser et al. argue for the visual system, Nelken describes for the auditory system how traditional approaches also lead to some misconceptions, due to the use of unnatural stimuli. Importantly, Nelken provides a working hypothesis for a hierarchical system of auditory processing stating that feature extraction is already achieved in the auditory system at pre-cortical levels — potentially a fundamental difference to the visual system — and auditory object formation is the main task of the primary auditory cortex. This is in line with increasing evidence for a complex context sensitivity in the auditory cortex, comparable only to that found in secondary cortical areas in the visual system (such as V1). To conclude this section of the issue, Olshausen and Field comment on the topic of sparse coding, the idea that only a few higher order sensory neurons represent relevant sensory information at any given point in time. This is again related to the question of context dependent processing of behaviorally relevant natural stimuli at higher stages of sensory processing. Although the concept of sparse coding is not new, there is increasing experimental evidence supporting it.
Context dependency, behavioral state and more Context dependent responses are not a sole characteristic of cortical areas. This is not a novel concept, but the review by Hurley et al. summarizes the dramatic success that has occurred in the field of neuromodulation. Focusing on serotonin and norepinephrine, they summarize some of the most important effects of neuromodulators on feature extraction neurons as well as on higher functions. In general, these effects are complex and go far beyond simple gain control functions, for instance, they differentially modulate specific properties of receptive fields. Thereby, they can alter the entire representation of a stimulus Current Opinion in Neurobiology 2004, 14:403–406
406 Sensory systems
feature in large populations of neurons, which can be directly related to the attentional state of an animal. A specific example of the effect of neuromodulators is discussed in the review by Prather and Mooney, who discuss recent progress in understanding the functional interplay among the different forebrain nuclei in the bird song system, in particular, in the context of recognition of conspecific songs. One of these nuclei, HVC and its inherent microcircuit, appears to be selectively reconfigured by the action of cholinergic and other neuromodulatory inputs, which depend on the bird’s behavioral state. Furthermore, the authors demonstrate the unrivaled conceptual beauty of the bird song system when it comes to understanding the interplay of learning, recognition, and resulting motor action and their neural substrates.
Influence of experience on sensory development and processing Pioneering experiments in the retina have revealed the influence of stimulation early in development of
Current Opinion in Neurobiology 2004, 14:403–406
peripheral organs on the development and maturation of sensory pathways. Grubb and Thompson review the large diversity of mechanisms by which the external environment, through early, and sometimes very early sensory activity and spontaneous activity, ensures appropriate maturation of sensory circuits. In addition to its mark on sensory pathway development, sensory experience also alters mature circuits, thus providing a basis for perceptual learning. In his review, Ghose provides an update on recent psychological and physiological studies addressing the variety of cortical processing strategies aimed at improving perceptual capabilities. Taken together, the current issue provides a cross section through recent advances in most sensory systems covering the broad range of levels in sensory processing from molecules up to perception. Nevertheless, we hope that it becomes apparent that there are some dominating themes crossing the bridges from one sense to others, as for instance in natural scene analysis.
www.sciencedirect.com