Systems Neurobiology: Plasticity in the Auditory System. Jason Middleton -

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1 Systems Neurobiology: Plasticity in the Auditory System Jason Middleton - jmiddlet@pitt.edu

2 Auditory plasticity Plasticity Early development and critical period Adult plasticity and neuromodulation Brainstem plasticity

3 Plasticity Substrate Mechanism Timescale Synapse Neuron Network Molecular Cellular Anatomical short, long

4 Short term synaptic plasticity Gil, et al. Neuron (1997) Reyes, et al. Nat Neurosci (1998)

5 Intrinsic property plasticity Song, et al. Nat Neurosci (2005)

6 Structural plasticity Trachtenberg, Nature (2002)

7 Plasticity Substrate Mechanism Timescale Synapse Neuron Network Molecular Cellular Anatomical short, long

8 Auditory system preferred frequency Hair cells Auditory stimulus frequency (khz) Caspary, et al. J Exp Biol (2008)

9 Polley, et al. J Neurophys (2007) - Cortex is tontopically organized along one dimension (tonotopic axis)

10 Polley, et al. J Neurophys (2007) - Different stimulus response properties obey different organizational principles in cortex

11 Auditory development and critical period When the effect of experience on the brain is particularly strong during a limited period in development, this period is referred to as a sensitive period. When experience provides information that is essential for normal development and alters performance permanently, such sensitive periods are referred to as critical periods. Knudsen, E. Journal of Cognitive Neuroscience (2004) Somatosensory: - critical period for barrel field development (P2-P5) Visual: - critical period for ocular dominance V1 (P15-P33)

12 Zhang, et al. Nat Neurosci (2001)

13 Zhang, et al. Nat Neurosci (2001)

14 Zhang, et al. Nat Neurosci (2001)

15 De Villers-Sidani, J Neurosci (2007) Critical period for auditory cortical tonotopic alignment: ~P11-P15

16 Chang, et al. Science (2003)

17 Chang, et al. Science (2003)

18 - Critical period for development of cortical tonotopy: ~P11-P15 - Tonotopy is plastic and can be altered by abnormal sensory experience - Auditory critical period can be extended by noise rearing - Normal tonotopy can be restored - Neural organization set up during critical period serves as a template for further adult plasticity

19 Adult cortical plasticity - Nucleus Basalis (NB); basal forebrain nucleus; major source of cholinergic input to cortex - Pairing NB electrical stimulation with acoustic tones causes overrepresentation in cortex Kilgard and Merzenich, Nature (1998) - What is the circuit basis for this reorganization?

20 Froemke, et al. Nature (2007)

21 Froemke, et al. Nature (2007)

22 Influence of operant learning r Bao, et al. Nature (2004)

23 Bao, et al. Nature (2004)

24 Bao, et al. Nature (2004) Bao, et al. Nature (2004)

25 Bao, et al. Nature (2004)

26 - Plasticity of neural representations auditory cortex extends in adulthood - Usually involves behaviorally relevant neuromodulation - Cholinergic modulation (Kilgard, Froemke, Merzenich) - Dopamine (Bao, Merzenich) - Norepinephrine, Oxytocin (Froemke, unpublished results)

27 Cortical plasticity... what about the brainstem?

28 Brainstem plasticity Song, et al. Nat Neurosci (2005) Seidl and Grothe J Neurophys (2005)

29 Bajo, et al. Nat Neurosci (2010) King, et al. Neurosci Biobehav Rev (2011)

30 King, et al. Neurosci Biobehav Rev (2011)

31 Bajo, et al. Nat Neurosci (2010) King, et al. Neurosci Biobehav Rev (2011)

32 Yan and Ehret, Eur J Neurosci (2002) Zhang, et al. Eur J Neurosci (2005)

33 Zhang, et al. Eur J Neurosci (2005)

34 Selected References development/critical period adult plasticity brainstem/midbrain Gil Z, Connors BW, Amitai Y. Differential regulation of neocortical synapses by neuromodulators and activity. Neuron, 19: (1997) Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, Sakmann B. Target-cell-specific facilitation and depression in neocortical circuits. Nature Neuroscience, 1: (1998) Song P, Yang Y, Barnes-Davies M, Bhattacharjee A, Hamann M, Forsythe ID, Oliver DL, Kaczmarek L. Acoustic environment determines phosphorylation state of the Kv3.1 potassium channel in auditory neurons. Nature Neuroscience, 8: (2005) Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, Welker E, Svoboda K. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature, 420: (2002) Caspary DM, Ling L, Turner JG, Hughes LF. Inhibitory neurotransmission, plasticity and aging in the mammalian central auditory system. Journal of Experimental Biology, 211: (2008) Polley DB, Read HL, Storace DA, Merzenich MM. Multiparametric auditory receptive field organization across five cortical fields in the albino rat. Journal of Neurophysiology, 97: (2007) Knudsen EI. Sensitive periods in the development of the brain and behavior. Journal of Cognitive Neuroscience, 16: (2004) Zhang LI, Bao S, Merzenich MM. Persistent influences of early acoustic environments on primary auditory cortex. Nature Neuroscience, 4: (2001) De Villers-Sidani E, Chang EF, Bao S, Merzenich MM. Critical period window for spectral tuning defined in the primary auditory cortex (A1) in the rat. Journal of Neuroscience, 27:180-9 (2007) Chang EF, Merzenich MM. Enviornmental noise retards auditory cortical development. Science, 300: (2003) Kilgard MP, Merzenich MM. Cortical map reorganization enabled by nucleus basalis activity. Science, 279: (1998) Froemke RC, Merzenich MM, Schreiner CE. A synaptic memory trace for cortical receptive field plasticity. Nature, 450: (2007) Bao S, Chang EF, Woods J, Merzenich MM. Temporal plasticity in the primary auditory cortex induced by operant learning. Nature Neuroscience, 7: (2004) Seidl AH and Grothe B. Development of sound localization mechanisms in the mongolian gerbil is shaped by early acoustic experience. Journal of Neurophysiology, 94: (2005) Bajo VM, Nodal FR, Moore DR, King AJ. The descending corticocollicular pathway mediates learning-induced auditory plasticity. Nature Neuroscience, 13: (2010) King AJ, Dahmen JC, Keating P, Leach ND, Nodal FR, Bajo VM. Neural circuits underlying adaptation and learning in the perception of auditory space. Neuroscience and Biobehavioral Reviews, 35: (2011) Yan J, Ehret G. Corticofugal modulation of midbrain sound processing in the house mouse. European Journal of Neuroscience, 16: (2002) Zhang Y, Hakes JJ, Bonfield SP, Yan J. Corticofugal feedback for auditory midbrain plasticity elicited by tones and electrical stimulation of basal forebrain in mice. European Journal of Neuroscience, 22: (2005)