The developmental origins of spatial navigation: Are we headed in the right direction?

Blumberg, Mark S.

doi:10.1016/j.tins.2015.01.001

Cited by 5 publications

(6 citation statements)

References 12 publications

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“…One possible explanation for the acute response is that the sudden loss of RN activity disinhibited other brainstem motor systems, which quickly compensated for that loss. A second possibility is that the increase in motor activity is the result of a sudden loss of RN activation of gamma motoneurons of muscle spindles (Appelberg, 1962). With a sudden loss of this fusimotor activation, muscle spindles would contract, thus reporting an apparent loss of muscle tone and thereby triggering a compensatory motor response.…”

Section: Discussionmentioning

confidence: 99%

Sensorimotor Processing in the Newborn Rat Red Nucleus during Active Sleep

Rio-Bermudez¹,

Sokoloff²,

Blumberg

2015

J. Neurosci.

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Sensory feedback from sleep-related myoclonic twitches is thought to drive activity-dependent development in spinal cord and brain. However, little is known about the neural pathways involved in the generation of twitches early in development. The red nucleus (RN), source of the rubrospinal tract, has been implicated in the production of phasic motor activity during active sleep in adults. Here we hypothesized that the RN is also a major source of motor output for twitching in early infancy, a period when twitching is an especially abundant motor behavior. We recorded extracellular neural activity in the RN during sleep and wakefulness in 1-week-old unanesthetized rats. Neurons in the RN fired phasically before twitching and wake movements of the contralateral forelimb. A subpopulation of neurons in the RN exhibited a significant peak of activity after forelimb movement onset, suggesting reafferent sensory processing. Consistent with this observation, manual stimulation of the forelimb evoked RN responses. Unilateral inactivation of the RN using a mixture comprising GABA A , GABA B , and glycine receptor agonists caused an immediate and temporary increase in motor activity followed by a marked and prolonged decrease in twitching and wake movements. Altogether, these data support a causal role for the RN in infant motor behavior. Furthermore, they indicate that twitching, which is characterized by discrete motor output and reafferent input, provides an opportunity for sensorimotor integration and activity-dependent development of topography within the newborn RN.

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Section: Discussionmentioning

confidence: 99%

Sensorimotor Processing in the Newborn Rat Red Nucleus during Active Sleep

Rio-Bermudez¹,

Sokoloff²,

Blumberg

2015

J. Neurosci.

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“…Here, we have presented the view that active sleep and twitching is key to the development of later-emerging spatial navigation abilities by providing a context for self-generated motor experiences that promote the emergence of long-range connectivity between the hippocampus with other key structures, including sensorimotor cortex (Del Rio-Bermudez et al, 2020;Mohns & Blumberg, 2010). Our approach contrasts with others that rely on the archaic concept of innateness to explain the development of this system (see Blumberg, 2015b).…”

Section: The Construction Of Embodimentmentioning

confidence: 99%

Sleep as a window on the sensorimotor foundations of the developing hippocampus

Rio-Bermudez

Blumberg

2021

Hippocampus

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The hippocampal formation plays established roles in learning, memory, and related cognitive functions. Recent findings also suggest that the hippocampus integrates sensory feedback from self‐generated movements to modulate ongoing motor responses in a changing environment. Such findings support the view of Bland and Oddie (Behavioural Brain Research, 2001, 127, 119–136) that the hippocampus is a site of sensorimotor integration. In further support of this view, we review neurophysiological evidence in developing rats that hippocampal function is built on a sensorimotor foundation and that this foundation is especially evident early in development. Moreover, at those ages when the hippocampus is first establishing functional connectivity with distant sensory and motor structures, that connectivity is preferentially expressed during periods of active (or REM) sleep. These findings reinforce the notion that sleep, as the predominant state of early infancy, provides a critical context for sensorimotor development, including development of the hippocampus and its associated network.

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“…During early life, the brain is also less-able to purposefully interact with the environment, as most sensory systems are not matured (Himwich, 1970; Jewett and Romano, 1972; Krug et al, 2001; Petersson et al, 2003; Colonnese et al, 2010), yet these systems display a variety of patterns of neural activity (Feller, 1999; Blankenship and Feller, 2009). There is a great deal of interest in this activity because it has been recognized to play essential roles in the normal development of the nervous system, acting in concert with genetically driven, molecular determinants of development (Goodman and Shatz, 1993; Tessier-Lavigne and Goodman, 1996; Chilton, 2006) to ensure formation of functional neural circuits (Pallas, 2001; Hanganu-Opatz, 2010; Blumberg, 2015). …”

Section: Spindle Bursts—a Key Pattern Of Spontaneous Activity In the mentioning

confidence: 99%

“…It is well established that, although the gross patterning of the somatosensory cortex may occur independently of activity, refinement relies on activity in the sensorimotor system (Pallas, 2001; Price et al, 2006; Inan and Crair, 2007; Hanganu-Opatz, 2010; Kolb et al, 2012; Blumberg, 2015; Cirelli and Tononi, 2015). In particular, injuring or deafferenting a limb during the first few days of life in the rat results in a failure of the development of the corresponding sensory cortex, as well as changes in sensory regions of the remaining limbs (Wall and Cusick, 1986; Dawson and Killackey, 1987; Waters et al, 1990; Pearson et al, 1999).…”

Section: Purpose Of Spindle Burstsmentioning

confidence: 99%

Large Scale Cortical Functional Networks Associated with Slow-Wave and Spindle-Burst-Related Spontaneous Activity

McVea

Murphy

Mohajerani

2016

Front. Neural Circuits

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Cortical sensory systems are active with rich patterns of activity during sleep and under light anesthesia. Remarkably, this activity shares many characteristics with those present when the awake brain responds to sensory stimuli. We review two specific forms of such activity: slow-wave activity (SWA) in the adult brain and spindle bursts in developing brain. SWA is composed of 0.5–4 Hz resting potential fluctuations. Although these fluctuations synchronize wide regions of cortex, recent large-scale imaging has shown spatial details of their distribution that reflect underlying cortical structural projections and networks. These networks are regulated, as prior awake experiences alter both the spatial and temporal features of SWA in subsequent sleep. Activity patterns of the immature brain, however, are very different from those of the adult. SWA is absent, and the dominant pattern is spindle bursts, intermittent high frequency oscillations superimposed on slower depolarizations within sensory cortices. These bursts are driven by intrinsic brain activity, which act to generate peripheral inputs, for example via limb twitches. They are present within developing sensory cortex before they are mature enough to exhibit directed movements and respond to external stimuli. Like in the adult, these patterns resemble those evoked by sensory stimulation when awake. It is suggested that spindle-burst activity is generated purposefully by the developing nervous system as a proxy for true external stimuli. While the sleep-related functions of both slow-wave and spindle-burst activity may not be entirely clear, they reflect robust regulated phenomena which can engage select wide-spread cortical circuits. These circuits are similar to those activated during sensory processing and volitional events. We highlight these two patterns of brain activity because both are prominent and well-studied forms of spontaneous activity that will yield valuable insights into brain function in the coming years.

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The developmental origins of spatial navigation: Are we headed in the right direction?

Cited by 5 publications

References 12 publications

Sensorimotor Processing in the Newborn Rat Red Nucleus during Active Sleep

Sensorimotor Processing in the Newborn Rat Red Nucleus during Active Sleep

Sleep as a window on the sensorimotor foundations of the developing hippocampus

Large Scale Cortical Functional Networks Associated with Slow-Wave and Spindle-Burst-Related Spontaneous Activity

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