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      The natural history of sound localization in mammals--a story of neuronal inhibition.

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          Abstract

          Our concepts of sound localization in the vertebrate brain are widely based on the general assumption that both the ability to detect air-borne sounds and the neuronal processing are homologous in archosaurs (present day crocodiles and birds) and mammals. Yet studies repeatedly report conflicting results on the neuronal circuits and mechanisms, in particular the role of inhibition, as well as the coding strategies between avian and mammalian model systems. Here we argue that mammalian and avian phylogeny of spatial hearing is characterized by a convergent evolution of hearing air-borne sounds rather than by homology. In particular, the different evolutionary origins of tympanic ears and the different availability of binaural cues in early mammals and archosaurs imposed distinct constraints on the respective binaural processing mechanisms. The role of synaptic inhibition in generating binaural spatial sensitivity in mammals is highlighted, as it reveals a unifying principle of mammalian circuit design for encoding sound position. Together, we combine evolutionary, anatomical and physiological arguments for making a clear distinction between mammalian processing mechanisms and coding strategies and those of archosaurs. We emphasize that a consideration of the convergent nature of neuronal mechanisms will significantly increase the explanatory power of studies of spatial processing in both mammals and birds.

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          Most cited references155

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          Normalization as a canonical neural computation.

          There is increasing evidence that the brain relies on a set of canonical neural computations, repeating them across brain regions and modalities to apply similar operations to different problems. A promising candidate for such a computation is normalization, in which the responses of neurons are divided by a common factor that typically includes the summed activity of a pool of neurons. Normalization was developed to explain responses in the primary visual cortex and is now thought to operate throughout the visual system, and in many other sensory modalities and brain regions. Normalization may underlie operations such as the representation of odours, the modulatory effects of visual attention, the encoding of value and the integration of multisensory information. Its presence in such a diversity of neural systems in multiple species, from invertebrates to mammals, suggests that it serves as a canonical neural computation.
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            Some general comments on the evolution and design of animal communication systems.

            Animal communication systems have evolved so that individuals can make decisions based upon the behaviour, physiology or morphology of others. Receiving mechanisms probably evolve to increase the efficiency and reliability of information reception whereas signals probably evolve to increase the efficiency of communication and reliability of manipulation of the receiving individual to the benefit of the emitter. The minimum requirement for clear reception suggests that any study of the evolution and design of communication systems must consider the factors that affect the quality of the received and processed signal. Critical information is needed about how the signal is generated and emitted, how it fares during transmission through air, water or substrate, how it is received and processed by the receiver's sensory and cognitive systems, and the factors which affect the fitness consequences of alternative ways of reacting to the information contained in the signal. These should allow predictions about the kinds and forms of signals used by animals signalling under known conditions. Phylogenetic history, and the geological time a clade spends in different signalling environments, will also affect signal evolution, and hence the success of predictions about signal design. We need to use methods of many different biological fields to understand the design and evolution of signals and signalling systems.
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              Sensory adaptation.

              Adaptation occurs in a variety of forms in all sensory systems, motivating the question: what is its purpose? A productive approach has been to hypothesize that adaptation helps neural systems to efficiently encode stimuli whose statistics vary in time. To encode efficiently, a neural system must change its coding strategy, or computation, as the distribution of stimuli changes. Information theoretic methods allow this efficient coding hypothesis to be tested quantitatively. Empirically, adaptive processes occur over a wide range of timescales. On short timescales, underlying mechanisms include the contribution of intrinsic nonlinearities. Over longer timescales, adaptation is often power-law-like, implying the coexistence of multiple timescales in a single adaptive process. Models demonstrate that this can result from mechanisms within a single neuron.
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                Author and article information

                Journal
                Front Neural Circuits
                Frontiers in neural circuits
                Frontiers Media SA
                1662-5110
                1662-5110
                2014
                : 8
                Affiliations
                [1 ] Division of Neurobiology, Department of Biology II, Ludwig Maximilians University Munich Munich, Germany.
                Article
                10.3389/fncir.2014.00116
                4181121
                25324726
                34959ae8-9413-4bec-99c8-d1f4fdba8fe8
                History

                GABA,LSO,MSO,archosaurs,binaural hearing,birds,evolution,glycine
                GABA, LSO, MSO, archosaurs, binaural hearing, birds, evolution, glycine

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