AMPA and GABAA/B receptor subunit expression in the cuneate nucleus of adult squirrel monkeys during peripheral nerve regeneration

Mowery, Todd M.; Kostylev, Polina V.; Garraghty, Preston E.

doi:10.1016/j.neulet.2013.11.054

Cited by 5 publications

(5 citation statements)

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“…As discussed for the cortex, the pattern of AMPA and GABA subunit distribution in the brainstem provide valuable insight into physiological states reported previously (Churchill et al, 2001; Garraghty and Churchill 2006). We also identify a very similar pattern of subunit expression observed 1 month after median nerve compression (Mowery et al, 2014). This suggests that brainstem plasticity at 1 to 5 yeas is not significantly different from the plasticity reported early after nerve injury (1 month).…”

Section: Discussionsupporting

confidence: 70%

“…GluR1 and presynaptic GABA B 1a show no change. This pattern of AMPA and GABA subunits is approximately similar to that seen during early reorganization (Mowery, Kostylev, and Garraghty 2014). This suggests that the cuneate nucleus enters a persistent state of heightened reorganizational plasticity.…”

Section: Introductionsupporting

confidence: 78%

“…This is followed by a subsequent phase of “developmental recapitulation” during which critical period like receptor expression (plasticity) is re-expressed in the deprived sensory neuraxis (Mowery and Garraghty, 2009; Mowery et al, 2011; Sarin et al, 2012). This phase could prime the cortex for the NMDA receptor-dependent stage of reorganization (Garraghty et al, 2006; Garraghty and Muja, 1996; Mowery et al, 2013; 2014 Myers et al, 2000). …”

Section: Introductionmentioning

confidence: 99%

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Differences in AMPA and GABAA/B receptor subunit expression between the chronically reorganized cortex and brainstem of adult squirrel monkeys

Mowery¹,

Sarin²,

Kostylev³

et al. 2015

Brain Research

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The primate somatosensory neuraxis provides a highly translational model system with which to investigate adult neural plasticity. Here, we report immunohistochemical staining data for AMPA and GABAA/B receptor subunits of area 3b cortex and cuneate nucleus of adult squirrel monkeys one to five years after median and ulnar nerve transection. In Area 3B cortex, the expression of GluR1 AMPAR subunits in reorganized regions are significantly increased, while the expression of GluR2/3 AMPAR subunits are not. GABAA α1 subunit expression in the reorganized region is not significantly different from control regions. Presynaptic GABABR1a subunit expression was also not significantly different between reorganized and control regions, while postsynaptic GABABR1b subunit expression was significantly decreased. In the cuneate nucleus of the brainstem, the expression of GluR1 AMPAR subunits in reorganized regions was not significantly different, while GluR2/3 AMPAR subunit expression was significantly elevated. GABAA α1 subunit expression in the reorganized region was significantly decreased. Presynaptic GABABR1a subunit expression was not significantly different, while postsynaptic GABABR1b subunit expression was significantly decreased. When subunit expression is compared, brainstem and cortical patterns diverge over longer periods of recovery. Persistent patterns of change in the cortex are stable by 1 year. Alternatively, subunit expression in the cuneate nucleus one to five years after nerve injury is similar to that seen 1 month after a reorganizing injury. This suggests that cortical plasticity continues to change over many months as receptive field reorganization occurs, while brainstem plasticity obtains a level of stable persistence by one month.

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Section: Discussionsupporting

confidence: 70%

Section: Introductionsupporting

confidence: 78%

Section: Introductionmentioning

confidence: 99%

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Differences in AMPA and GABAA/B receptor subunit expression between the chronically reorganized cortex and brainstem of adult squirrel monkeys

Mowery¹,

Sarin²,

Kostylev³

et al. 2015

Brain Research

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“…These authors also suggest that the latter findings are suggestive of a “trace” of the chronic stimulation (cf. [ 4 , 5 ]). Such “traces” would also seem to pose a challenge for purely homeostatic mechanisms.…”

Section: In Vivo Homeostatic Plasticity Experimmentioning

confidence: 99%

Reconciling Homeostatic and Use-Dependent Plasticity in the Context of Somatosensory Deprivation

Orczyk

Garraghty

2015

Neural Plasticity

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The concept of homeostatic plasticity postulates that neurons maintain relatively stable rates of firing despite changing inputs. Homeostatic and use-dependent plasticity mechanisms operate concurrently, although they have different requirements for induction. Depriving central somatosensory neurons of their primary activating inputs reduces activity and results in compensatory changes that favor excitation. Both a reduction of GABAergic inhibition and increase in glutamatergic excitatory transmission are observed in input-deprived cortex. Topographic reorganization of the adult somatosensory cortex is likely driven by both homeostatic and use-dependent mechanisms. Plasticity is induced by changes in the strengths of synaptic inputs, as well as changes in temporal correlation of neuronal activity. However, there is less certainty regarding the in vivo contribution of homeostatic mechanisms as in vitro experiments rely on manipulations that create states that do not normally occur in the living nervous system. Homeostatic plasticity seems to occur, but more in vivo research is needed to determine mechanisms. In vitro research is also needed but should better conform to conditions that might occur naturally in vivo.

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“…An important component of the model was the learning process that we envisage to be one of the earliest developmental steps toward a functional tactile neural system. Although there are several indications that the PA synapses on the cuneate neurons are extensively plastic at least during some phase of development (Bengtsson et al, 2013 ) and following removal of PA inputs (Kambi et al, 2014 ; Mowery et al, 2014 ), the direct synaptic mechanisms underlying the plasticity have not been explored. Therefore, in order to model this learning process, we used an already validated idea of a calcium activity-dependent mechanism (Helias et al, 2008 ), which to some extent can be regarded a general synaptic plasticity mechanisms of neurons.…”

Section: Discussionmentioning

confidence: 99%

Intracellular Dynamics in Cuneate Nucleus Neurons Support Self-Stabilizing Learning of Generalizable Tactile Representations

Rongala

Spanne

Mazzoni

et al. 2018

Front. Cell. Neurosci.

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How the brain represents the external world is an unresolved issue for neuroscience, which could provide fundamental insights into brain circuitry operation and solutions for artificial intelligence and robotics. The neurons of the cuneate nucleus form the first interface for the sense of touch in the brain. They were previously shown to have a highly skewed synaptic weight distribution for tactile primary afferent inputs, suggesting that their connectivity is strongly shaped by learning. Here we first characterized the intracellular dynamics and inhibitory synaptic inputs of cuneate neurons in vivo and modeled their integration of tactile sensory inputs. We then replaced the tactile inputs with input from a sensorized bionic fingertip and modeled the learning-induced representations that emerged from varied sensory experiences. The model reproduced both the intrinsic membrane dynamics and the synaptic weight distributions observed in cuneate neurons in vivo. In terms of higher level model properties, individual cuneate neurons learnt to identify specific sets of correlated sensors, which at the population level resulted in a decomposition of the sensor space into its recurring high-dimensional components. Such vector components could be applied to identify both past and novel sensory experiences and likely correspond to the fundamental haptic input features these neurons encode in vivo. In addition, we show that the cuneate learning architecture is robust to a wide range of intrinsic parameter settings due to the neuronal intrinsic dynamics. Therefore, the architecture is a potentially generic solution for forming versatile representations of the external world in different sensor systems.

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AMPA and GABAA/B receptor subunit expression in the cuneate nucleus of adult squirrel monkeys during peripheral nerve regeneration

Cited by 5 publications

References 115 publications

Differences in AMPA and GABAA/B receptor subunit expression between the chronically reorganized cortex and brainstem of adult squirrel monkeys

Differences in AMPA and GABAA/B receptor subunit expression between the chronically reorganized cortex and brainstem of adult squirrel monkeys

Reconciling Homeostatic and Use-Dependent Plasticity in the Context of Somatosensory Deprivation

Intracellular Dynamics in Cuneate Nucleus Neurons Support Self-Stabilizing Learning of Generalizable Tactile Representations

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