TY - JOUR
T1 - TrkB activation during a critical period mimics the protective effects of early visual experience on perception and the stability of receptive fields in adult superior colliculus
AU - Mudd, David B.
AU - Balmer, Timothy S.
AU - Kim, So Yeon
AU - Machhour, Noura
AU - Pallas, Sarah L.
N1 - Funding Information:
This work was supported by a Georgia State University Brains and Behavior Fellowship and a Georgia State University Center for Neuromics student grant to D.B.M., and a Georgia State University Brains and Behavior seed grant, National Science Foundation Grant IOS-1656838, and DARPA Grant HR0011-18-2-0019, TA2 to S.L.P. We thank Dr. Angela Mabb (Georgia State University Neuroscience Department) and Dr. Hyuk-Kyu Seoh (Georgia State UniversityBiologyDepartment)forprovidingguidanceonWesternblotimagingandanalysis;membersoftheS.L.P. laboratory for technical support and manuscript review; and the Department of Animal Resources staff at Georgia State University for excellent animal care. The authors declare no competing financial interests. Correspondence should be addressed to Sarah L. Pallas at spallas@umass.edu.
Publisher Copyright:
© 2019 the authors.
PY - 2019/6/5
Y1 - 2019/6/5
N2 - During a critical period in development, spontaneous and evoked retinal activity shape visual pathways in an adaptive fashion. Interestingly, spontaneous activity is sufficient for spatial refinement of visual receptive fields (RFs) in superior colliculus (SC) and visual cortex (V1), but early visual experience is necessary to maintain inhibitory synapses and stabilize RFs in adulthood (Carrasco et al., 2005, 2011; Carrasco and Pallas, 2006; Balmer and Pallas, 2015a). In V1, BDNF and its high-affinity receptor TrkB are important for development of visual acuity, inhibition, and regulation of the critical period for ocular dominance plasticity (Hanover et al., 1999; Huang et al., 1999; Gianfranceschi et al., 2003). To examine the generality of this signaling pathway for visual system plasticity, the present study examined the role of TrkB signaling during the critical period for RF refinement in SC. Activating TrkB receptors during the critical period (P33-P40) in dark reared subjects produced normally refined RFs, and blocking TrkB receptors in light-exposed animals resulted in enlarged adult RFs like those in dark reared animals. We also report here that deprivation-or TrkB blockade-induced RF enlargement in adulthood impaired fear responses to looming overhead stimuli and negatively impacted visual acuity. Thus, early TrkB activation is both necessary and sufficient to maintain visual RF refinement, robust looming responses, and visual acuity in adulthood. These findings suggest a common signaling pathway exists for the maturation of inhibition between V1 and SC.
AB - During a critical period in development, spontaneous and evoked retinal activity shape visual pathways in an adaptive fashion. Interestingly, spontaneous activity is sufficient for spatial refinement of visual receptive fields (RFs) in superior colliculus (SC) and visual cortex (V1), but early visual experience is necessary to maintain inhibitory synapses and stabilize RFs in adulthood (Carrasco et al., 2005, 2011; Carrasco and Pallas, 2006; Balmer and Pallas, 2015a). In V1, BDNF and its high-affinity receptor TrkB are important for development of visual acuity, inhibition, and regulation of the critical period for ocular dominance plasticity (Hanover et al., 1999; Huang et al., 1999; Gianfranceschi et al., 2003). To examine the generality of this signaling pathway for visual system plasticity, the present study examined the role of TrkB signaling during the critical period for RF refinement in SC. Activating TrkB receptors during the critical period (P33-P40) in dark reared subjects produced normally refined RFs, and blocking TrkB receptors in light-exposed animals resulted in enlarged adult RFs like those in dark reared animals. We also report here that deprivation-or TrkB blockade-induced RF enlargement in adulthood impaired fear responses to looming overhead stimuli and negatively impacted visual acuity. Thus, early TrkB activation is both necessary and sufficient to maintain visual RF refinement, robust looming responses, and visual acuity in adulthood. These findings suggest a common signaling pathway exists for the maturation of inhibition between V1 and SC.
KW - Adult plasticity
KW - Inhibitory plasticity
KW - Retinotectal
KW - Sensory deprivation
KW - Synaptic plasticity
KW - Visual development
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U2 - 10.1523/JNEUROSCI.2598-18.2019
DO - 10.1523/JNEUROSCI.2598-18.2019
M3 - Article
C2 - 30940716
AN - SCOPUS:85067373628
SN - 0270-6474
VL - 39
SP - 4475
EP - 4488
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 23
ER -