A revised view of sensory cortical parcellation

Wallace, Mark T.; Ramachandran, Ramnarayan; Stein, Barry E.

doi:10.1073/pnas.0305697101

Cited by 308 publications

(242 citation statements)

References 43 publications

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“…Studies of visual (55) and somatosensory (30,53) pathways demonstrate the presence of thalamic bursting in awake and attentive states, implying that bursting activity modulates sensory perception. Intermittent activation of multiple long-range circuits to integrate major sensory cortices suggests that multisensory integration is essential to shape sensory perceptions that could not otherwise be achieved with only one sense (56,57). This premise raises an intriguing proposition that excitatory long-range projections and their dynamic interactions are recruited during low-frequency thalamic stimulation through burst activity propagation from VPM to S1 and, possibly, to other sensory cortices.…”

Section: Discussionmentioning

confidence: 99%

Long-range projections coordinate distributed brain-wide neural activity with a specific spatiotemporal profile

Leong

Chan

Gao

et al. 2016

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

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One challenge in contemporary neuroscience is to achieve an integrated understanding of the large-scale brain-wide interactions, particularly the spatiotemporal patterns of neural activity that give rise to functions and behavior. At present, little is known about the spatiotemporal properties of long-range neuronal networks. We examined brain-wide neural activity patterns elicited by stimulating ventral posteromedial (VPM) thalamo-cortical excitatory neurons through combined optogenetic stimulation and functional MRI (fMRI). We detected robust optogenetically evoked fMRI activation bilaterally in primary visual, somatosensory, and auditory cortices at low (1 Hz) but not high frequencies (5-40 Hz). Subsequent electrophysiological recordings indicated interactions over long temporal windows across thalamo-cortical, cortico-cortical, and interhemispheric callosal projections at low frequencies. We further observed enhanced visually evoked fMRI activation during and after VPM stimulation in the superior colliculus, indicating that visual processing was subcortically modulated by low-frequency activity originating from VPM. Stimulating posteromedial complex thalamo-cortical excitatory neurons also evoked brain-wide bloodoxygenation-level-dependent activation, although with a distinct spatiotemporal profile. Our results directly demonstrate that lowfrequency activity governs large-scale, brain-wide connectivity and interactions through long-range excitatory projections to coordinate the functional integration of remote brain regions. This low-frequency phenomenon contributes to the neural basis of long-range functional connectivity as measured by resting-state fMRI.fMRI | optogenetic | brain connectivity | low frequency | thalamus T he brain is a highly complex, interconnected structure with parallel and hierarchical networks distributed within and between neural systems (1, 2). This integrative architecture dictates the underlying principles of how brain-wide neural connectivity supports and organizes sensory, behavioral, and cognitive processes (3). Recent advances in structural (2, 4) and functional connectivity (5-12) mapping, as well as neural circuit modulatory tools, such as optogenetics (13, 14), permit detailed, high-resolution neural examinations at unprecedented scales. In particular, functional connectivity mapping using resting-state functional MRI (rsfMRI) produces noninvasive visualization of slow and spontaneous hemodynamic fluctuations in humans (5-9) and animals (10-12). Coherent low-frequency (<1 Hz) fluctuations across functionally coupled, large-scale networks is an intriguing property, although the exact underlying neural bases and functional significance remain unclear. Previous studies integrating large-scale electrical recordings, voltage-sensitive dye (VSD), and Ca 2+ -imaging techniques (15-18) support the hypothesis that slow, oscillating neural activity constrains and elicits these hemodynamic fluctuations. Furthermore, low-frequency activity can temporally synchronize remote brain region...

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Section: Discussionmentioning

confidence: 99%

Long-range projections coordinate distributed brain-wide neural activity with a specific spatiotemporal profile

Leong

Chan

Gao

et al. 2016

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

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“…Such a spatial organization was not violated during development, perhaps be- cause this fundamental feature of cortical organization (Barth et al, 1993;Wallace et al, 2004a) (but see Ghazanfar and Schroeder, 2006) is established even before the networks are responsive to sensory stimuli. The sensory chronology of AES appears to follow a pattern closely paralleling that found in its major subcortical target structure, the SC (Stein et al, 1973).…”

Section: Discussionmentioning

confidence: 99%

The Development of Cortical Multisensory Integration

Wallace

Carriere²,

Perrault³

et al. 2006

J. Neurosci.

117

120

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Although there are many perceptual theories that posit particular maturational profiles in higher-order (i.e., cortical) multisensory regions, our knowledge of multisensory development is primarily derived from studies of a midbrain structure, the superior colliculus. Therefore, the present study examined the maturation of multisensory processes in an area of cat association cortex [i.e., the anterior ectosylvian sulcus (AES)] and found that these processes are rudimentary during early postnatal life and develop only gradually thereafter. The AES comprises separate visual, auditory, and somatosensory regions, along with many multisensory neurons at the intervening borders between them. During early life, sensory responsiveness in AES appears in an orderly sequence. Somatosensory neurons are present at 4 weeks of age and are followed by auditory and multisensory (somatosensory-auditory) neurons. Visual neurons and visually responsive multisensory neurons are first seen at 12 weeks of age. The earliest multisensory neurons are strikingly immature, lacking the ability to synthesize the cross-modal information they receive. With postnatal development, multisensory integrative capacity matures. The delayed maturation of multisensory neurons and multisensory integration in AES suggests that the higher-order processes dependent on these circuits appear comparatively late in ontogeny.

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“…5A-D, gray connections). The DGZ neurons respond to both whisker and auditory stimuli (Brett-Green et al, 2003;Wallace et al, 2004). The DGZ receives auditory input from A1 cortex, from the ventral division of the MGN, and also from the multisensory neurons in the mMGN (Brett-Green et al, 2003).…”

Section: Discussionmentioning

confidence: 99%

Cross-Sensory Modulation of Primary Sensory Cortex Is Developmentally Regulated by Early Sensory Experience

Ghoshal¹,

Tomarken²,

Ebner³

2011

J. Neurosci.

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The presence of cross-sensory influences on neuronal responses in primary sensory cortex has been observed previously using several different methods. To test this idea in rat S1 barrel cortex, we hypothesized that auditory stimuli combined with whisker stimulation ("cross-sensory" stimuli) may modify response levels to whisker stimulation. Since the brain has been shown to have a remarkable capacity to be modified by early postnatal sensory activity, manipulating postnatal sensory experiences would be predicted to alter the degree of cross-sensory interactions. To test these ideas, we raised rats with or without whisker deprivation and with or without postnatal exposure to repeated auditory clicks. We recorded extracellular responses under urethane anesthesia from barrel cortex neurons in response to principal whisker stimulation alone, to auditory click stimulation alone, or to a cross-sensory stimulus. The responses were compared statistically across different stimulus conditions and across different rearing groups. Barrel neurons did not generate action potentials in response to auditory click stimuli alone in any rearing group. However, in cross-sensory stimulus conditions the response magnitude was facilitated in the 0 -15 ms post-whisker-stimulus epoch in all rearing conditions, whereas modulation of response magnitude in a later 15-30 ms post-whisker-stimulus epoch was significantly different in each rearing condition. The most significant cross-sensory effect occurred in rats that were simultaneously whisker deprived and click reared. We conclude that there is a modulatory type of cross-sensory auditory influence on normal S1 barrel cortex, which can be enhanced by early postnatal experiences.

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A revised view of sensory cortical parcellation

Cited by 308 publications

References 43 publications

Long-range projections coordinate distributed brain-wide neural activity with a specific spatiotemporal profile

Long-range projections coordinate distributed brain-wide neural activity with a specific spatiotemporal profile

The Development of Cortical Multisensory Integration

Cross-Sensory Modulation of Primary Sensory Cortex Is Developmentally Regulated by Early Sensory Experience

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