Auditory thalamus integrates visual inputs into behavioral gains

Komura, Yutaka; Tamura, Ryoi; Uwano, Teruko; Nishijo, Hisao; Ono, Taketoshi

doi:10.1038/nn1528

Cited by 105 publications

(79 citation statements)

References 52 publications

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“…The observed behavioral increase in sensitivity across modalities seems to originate at least partially from the interaction in a primary sensory integration center, and similar phenomena have so far only been described in higher-order brain centers in vertebrates (17,18). Interestingly, the change in sensitivity of MGC neurons after sound exposure seems to occur in a bimodal manner.…”

Section: Discussionsupporting

confidence: 66%

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Brief predator sound exposure elicits behavioral and neuronal long-term sensitization in the olfactory system of an insect

Anton¹,

Evengaard

Barrozo

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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Modulation of sensitivity to sensory cues by experience is essential for animals to adapt to a changing environment. Sensitization and adaptation to signals of the same modality as a function of experience have been shown in many cases, and some of the neurobiological mechanisms underlying these processes have been described. However, the influence of sensory signals on the sensitivity of a different modality is largely unknown. In males of the noctuid moth, Spodoptera littoralis, the sensitivity to the femaleproduced sex pheromone increases 24 h after a brief preexposure with pheromone at the behavioral and central nervous level. Here we show that this effect is not confined to the same sensory modality: the sensitivity of olfactory neurons can also be modulated by exposure to a different sensory stimulus, i.e., a pulsed stimulus mimicking echolocating sounds from attacking insectivorous bats. We tested responses of preexposed male moths in a walking bioassay and recorded from neurons in the primary olfactory center, the antennal lobe. We show that brief exposure to a bat call, but not to a behaviorally irrelevant tone, increases the behavioral sensitivity of male moths to sex pheromone 24 h later in the same way as exposure to the sex pheromone itself. The observed behavioral modification is accompanied by an increase in the sensitivity of olfactory neurons in the antennal lobe. Our data provide thus evidence for cross-modal experience-dependent plasticity not only on the behavioral level, but also on the central nervous level, in an insect.bat sound | plant odor | sexual behavior | intracellular recording A nimals live in an ever-changing environment and must be able to adapt their behavior in response to highly varying sensory cues. One way to achieve such adaptive behavior is through plasticity of the nervous system, whereby modifications can be induced depending on sensory input. Previous studies have shown that exposure to environmental signals during development and in early adult life might influence the precise design and sensitivity of the targeted sensory system (1-3). The development of the peripheral and central visual, auditory, somatosensory, and olfactory systems in vertebrates has been shown to be highly influenced by experience (e.g., refs. 4-11) and regulated by neurogenesis and network remodeling with, for example, axon growth, the increase of the number of synaptic connections, and the strengthening of existing synapses (ref. 1 and references therein; ref. 12).Different strategies to achieve high sensitivity for abundant and/ or important signals have evolved. One way is limited attention, whereby an animal focuses on a specific sensory system, or even on a specific type of sensory signal, whereas other, simultaneously occurring information signals might be less attended (13,14). Experience of sensory input with a behaviorally important stimulus could also elicit long-term changes, which improve the insect's ability to respond to that specific stimulus (e.g., ref. 15). Furthermore, brief s...

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Section: Discussionsupporting

confidence: 66%

“…16 and references therein describe studies on the marine mollusk Aplysia) but can also lead to a higher sensitivity for an attractive stimulus. Such phenomena have been found in vertebrates, including humans, in which cross-modal sensory input influences the central processing of stimuli perceived through different input channels (17,18).…”

mentioning

confidence: 92%

Brief predator sound exposure elicits behavioral and neuronal long-term sensitization in the olfactory system of an insect

Anton¹,

Evengaard

Barrozo

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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“…Recently, Komura et al (2001Komura et al ( , 2005 observed similar activity in the rat auditory thalamus (i.e., a gradual increase in neural activity during trials that terminated with the trial). In addition, they demonstrated that this "late response" could be modulated by reward value.…”

Section: Discussionmentioning

confidence: 79%

“…Another possibility exists with descending connections within the auditory pathway. Reward-related activity that was observed in thalamic neurons (Komura et al, 2001(Komura et al, , 2005 may be transmitted to the IC (Adams, 1980;Kuwabara and Zook, 2000;Winer et al, 2002). Additional task-related signals have been reported in auditory cortex (Durif et al, 2003;Brosch et al, 2005); these too could be transmitted to the IC via descending projections (Huffman and Henson, 1990).…”

Section: Discussionmentioning

confidence: 87%

Effects of Reward and Behavioral Context on Neural Activity in the Primate Inferior Colliculus

2006

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Neural activity in the inferior colliculus (IC) likely plays an integral role in the processing of various auditory parameters, such as sound location and frequency. However, little is known about the extent to which IC neural activity may be influenced by the context in which sounds are presented. In this study, we examined neural activity of IC neurons in the rhesus monkey during an auditory task in which a sound served as a localization target for a saccade. Correct performance was rewarded, and the magnitude of the reward was varied in some experiments. Neural activity was also assessed during a task in which the monkey maintained fixation of a light while ignoring the sound, as well as when sounds were presented in the absence of any task. We report that neural activity increased late in the trial in the saccade task in 58% of neurons and that the level of activity throughout the trials could be modulated by reward magnitude for many neurons. The late-trial neural activity similarly increased in the fixation task in 39% of the neurons tested for this task but was not observed when sounds were presented in the absence of a behavioral task and reward. Together, these results suggest that a rewardrelated signal influences neural activity in the IC.

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“…Moreover, thalamic neurons seem to modulate their response to auditory stimuli depending on the congruency of visual co-stimulation [47].…”

Section: The Multisensory Brainmentioning

confidence: 99%

Multisensory integration and neuroplasticity in the human cerebral cortex

Paraskevopoulos

Herholz

2013

Translational Neuroscience

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There is a strong interaction between multisensory processing and the neuroplasticity of the human brain. On one hand, recent research demonstrates that experience and training in various domains modifies how information from the different senses is integrated; and, on the other hand multisensory training paradigms seem to be particularly effective in driving functional and structural plasticity. Multisensory training affects early sensory processing within separate sensory domains, as well as the functional and structural connectivity between uniand multisensory brain regions. In this review, we discuss the evidence for interactions of multisensory processes and brain plasticity and give an outlook on promising clinical applications and open questions.

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Auditory thalamus integrates visual inputs into behavioral gains

Cited by 105 publications

References 52 publications

Brief predator sound exposure elicits behavioral and neuronal long-term sensitization in the olfactory system of an insect

Brief predator sound exposure elicits behavioral and neuronal long-term sensitization in the olfactory system of an insect

Effects of Reward and Behavioral Context on Neural Activity in the Primate Inferior Colliculus

Multisensory integration and neuroplasticity in the human cerebral cortex

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