Behavioral States Modulate Sensory Processing in Early Development

Dooley, James C.; Sokoloff, Greta; Blumberg, Mark S.

doi:10.1007/s40675-019-00144-z

Cited by 5 publications

(4 citation statements)

References 61 publications

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“…However, other studies claim that behavioral state moderates the relationship between movement and cortical activity [5][6][7]. Thus, perhaps inattention to behavioral state leads to failures to detect movement-driven activity [8]. Here, we resolve this issue by associating local field activity (i.e., spindle bursts) and unit activity in the barrel cortex of 5-day-old rats with whisker movements during wake and myoclonic twitches of the whiskers during active (REM) sleep.…”

Section: Discussionmentioning

confidence: 86%

Self-Generated Whisker Movements Drive State-Dependent Sensory Input to Developing Barrel Cortex

et al. 2020

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Section: Discussionmentioning

confidence: 86%

Self-Generated Whisker Movements Drive State-Dependent Sensory Input to Developing Barrel Cortex

et al. 2020

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mentioning

confidence: 86%

Self-generated whisker movements drive state-dependent sensory input to developing barrel cortex

Dooley

Glanz

Sokoloff

et al. 2020

Preprint

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SummaryCortical development is an activity-dependent process [1–3]. Regarding the role of activity in developing somatosensory cortex, one persistent debate concerns the importance of sensory feedback from self-generated movements. Specifically, recent studies claim that cortical activity is generated intrinsically, independent of movement [3, 4]. However, other studies claim that behavioral state moderates the relationship between movement and cortical activity [5–7]. Thus, perhaps inattention to behavioral state leads to failures to detect movement-driven activity [8]. Here, we resolve this issue by associating local field activity (i.e., spindle bursts) and unit activity in the barrel cortex of 5-day-old rats with whisker movements during wake and myoclonic twitches of the whiskers during active (REM) sleep. Barrel activity increased significantly within 500 ms of whisker movements, especially after twitches. Also, higher-amplitude movements were more likely to trigger barrel activity; when we controlled for movement amplitude, barrel activity was again greater after a twitch than a wake movement. We then inverted the analysis to assess the likelihood that increases in barrel activity were preceded within 500 ms by whisker movements: At least 55% of barrel activity was attributable to sensory feedback from whisker movements. Finally, when periods with and without movement were compared, 70–75% of barrel activity was movement-related. These results confirm the importance of sensory feedback from movements in driving activity in sensorimotor cortex and underscore the necessity of monitoring sleep-wake states to ensure accurate assessments of the contributions of the sensory periphery to activity in developing somatosensory cortex.

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“…Twitches are spontaneous limb jerks that dominate during active sleep, whereas long-lasting and complex movements more often occur during waking periods. Although both sleep and waking movements trigger reafferent signals, the ensuing activation of the ascending pathways is state-dependent (Dooley et al, 2019). In sleeping states, twitches evoke responses in the somatosensory thalamus, cortex, and motor cortex (Khazipov et al, 2004;McVea et al, 2012), whereas waking movements fail to evoke any supraspinal response (Tiriac et al, 2012; or they evoke only poorly reliable responses, such as those related to whisker movements (Dooley et al, 2020).…”

Section: From the Sensorimotor Systemmentioning

confidence: 99%

Spontaneous activity in developing thalamic and cortical sensory networks

Martini

Guillamón-Vivancos

Moreno‐Juan

et al. 2021

Neuron

116

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Developing sensory circuits exhibit different patterns of spontaneous activity, patterns that are related to the construction and refinement of functional networks. During the development of different sensory modalities, spontaneous activity originates in the immature peripheral sensory structures and in the higher-order central structures, such as the thalamus and cortex. Certainly, the perinatal thalamus exhibits spontaneous calcium waves, a pattern of activity that is fundamental for the formation of sensory maps and for circuit plasticity. Here, we review our current understanding of the maturation of early (including embryonic) patterns of spontaneous activity and their influence on the assembly of thalamic and cortical sensory networks. Overall, the data currently available suggest similarities between the developmental trajectory of brain activity in experimental models and humans, which in the future may help to improve the early diagnosis of developmental disorders.

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Behavioral States Modulate Sensory Processing in Early Development

Cited by 5 publications

References 61 publications

Self-Generated Whisker Movements Drive State-Dependent Sensory Input to Developing Barrel Cortex

Self-Generated Whisker Movements Drive State-Dependent Sensory Input to Developing Barrel Cortex

Self-generated whisker movements drive state-dependent sensory input to developing barrel cortex

Spontaneous activity in developing thalamic and cortical sensory networks

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