Mechanisms of plasticity in the developing visual cortex and how behavioral state changes cortical gain and adult plasticity
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1 Mechanisms of plasticity in the developing visual cortex and how behavioral state changes cortical gain and adult plasticity Michael P. Stryker Center for Integrative Neuroscience University of California, San Francisco University of Science and Technology of China Hefei, China May, 2014
2 Stages of Development of Mouse Primary Visual Cortex (V1)
3 Mechanisms responsible for topographic maps.
4 At least some maps are essentially perfect. Example: the retinogeniculate map evidence physiology that multi-input RFs are perfectly compact, and many single-input RFs.
5 How can we reconcile this precision seen in physiology with the shaggy axonal and dendritic arbors seen by anatomy? The apparent precision in connectivity is much better than the size of the axonal or dendritic arbors.
6 Precision ~ 0.1% Precision ~ 5%, apparently
7 What signal is present at the cells of origin that could be used to attain such precision of connections in the target structure? Neural activity is such a signal. Willshaw, D. J & von der Malsburg, C. (1976) How Patterned Neural Connections Can Be Set Up by Self- Organization. PRSB 194: showed that maps can be set up by either chemical labels that are shared among neighbors or by neural activity. (board)
8 Correlated activity of neighbors in the input array plus a reinforcement of the connections that are effective in driving the target cells can produce map refinement. Hebb s rule. Input far away output
9 The first Simple Cell, from Hubel & Wiesel (1959) Orientation selectivity (1962) Alonso & Reid (1995) Nature
10 Ocular Dominance in the Cat
11 Human Ocular Dominance Columns Columns marked by metabolic stain after loss of one eye shortly before death, in tangential section through cortical input layer IV. Series of sections drawn onto postmortem photograph of brain Courtesy of Dr. Jonathan Horton, UCSF
12 Ocular Dominance Plasticity in the Cat
13 Earlier work had shown that the change in thalamocortical input to ocular dominance columns in layer 4 of cortex took a week, and resulted in the loss of at least half the input. 0.5 mm Antonini & Stryker, Science Changes in the visual responses of layer 4 neurons also took several days. The process was competitive: closing both eyes or even blocking all cortical activity with TTX did not cause such shrinkage
14 Beyond the input layer of the cortex, physiological changes in responses to the two eyes were much faster, taking only 1-2 days. f o f o t n e c r e P days t n e c r e P The inability to manipulate directly the signals that neurons send and receive made it hard to discover the mechanisms of plasticity in carnivores and primates. Trachtenberg & Stryker, J Neurosci
15 We now mostly study mice. Soe how good is the mouse cortex as a model for the human s? How does action affect perception and plasticity? Can we study its effects in the mouse? What s next?
16 A few prominent differences between mouse and human (or other higher primate) visual cortex. Mouse and other rodents lack orientation and ocular dominance columns. Many compelling similarities. Same basic structure and cell types as defined by morphology, inputs and outputs, and in may cases gene expression. Similar sequence of developmental events. Both have multiple visual areas, dorsal and ventral streams. Similar response properties and receptive fields of single neurons. Similar activity-dependent plasticity.
17 Retino-geniculo-cortical pathway in the mouse monocular binocular primary visual cortex (V1) dorsal lateral geniculate nucleus (dlgn)
18 Percent of Cells Percent of Cells But mouse V1 does have rapid ocular dominance plasticity following monocular deprivation (MD) mean score mean score MD 4 days Ocular Dominance Score contra ipsi Ocular Dominance Score contra ipsi Gordon and Stryker, 1996
19 Ocular dominance plasticity induced by short MD in mouse V1 has a well defined critical period P25-P28 Gordon & Stryker, 1996 Prusky et al, 2000
20 Putative excitatory and inhibitory neurons have distinct spikes Multi-site silicon probes essential for studying units with low spontaneous rates, for measuring consistent spike shapes, for CSD, and for validating cortical state. Niell & Stryker, 2008
21 The mouse simple cell receptive fields are as pretty as those in cats and monkeys Niell & Stryker, 2008
22 Most excitatory neurons are highly selective for orientation Niell & Stryker, 2008
23 Gabor parameters of Monkey, Cat and Mouse RFs
24 Most excitatory neurons are highly linear and show highly sophisticated features, such as contrast-invariant orientation tuning Niell & Stryker, 2008
25 Mouse visual cortex lacks orientation and ocular dominance columns
26 Mouse experiments revealed what the critical period is for: binocular matching of orientation selectivity Wang Sarnaik & Cang, 2010
27 Optical Imaging of Intrinsic Signals Intrinsic signals = changes in light reflectance in brain tissue due to hemodynamic responses evoked by neural activity Most important factor is greater absorption of red light by deoxyhemoglobin than oxyhemoglobin (Bonhoeffer and Grinvald, 1996). CCD camera Modified from Hillman 2007
28 Measuring visual responses using intrinsic signal imaging binocular + monocular areas binocular area 30 cm 77 Contra (right) eye stimulation Ipsi eye stim. 20 Contra eye stim. 1 mm image through intact skull 1 mm R/R x10 4 Ocular dominance index (ODI) = (C-I) / (C+I)
29 Change in response amplitude Tracking changes in responses in individual animals during MD and after re-opening Response amplitude ( R/Rx10 4 ) Contralateral eye (closed) Ipsilateral eye (open) closed-eye open-eye 1. Loss of response to deprived eye 2. Increase in response to open eye 3. Restoration of the original condition after ending deprivation baseline MD2-3 MD5-6 recovery day day 4 day baseline MD2-3d MD5-6d Recovery MD Binocular vision Re-open closed eye
30 Change in response amplitude previous studies Summary Ca ++, CamKII, NMDA-R Inhibition closed-eye open-eye TNFα TrkB baseline MD2-3d MD5-6d Recovery
31 Change in response amplitude previous studies and Hypothesis Ca ++, CamKII, NMDA-R Inhibition closed-eye open-eye TNFα TrkB baseline MD2-3d MD5-6d Recovery Hypothesis Loss of synapses in closed-eye circuit TNFα-mediated homeostatic synaptic scaling Re-growth of synapses in reopened-eye circuit
32 Next step: Measure rewiring of the different cortical circuits directly while manipulating signaling mechanisms specifically in specific cell types Espinosa & Stryker, unpublished, 2013
33 Espinosa & Stryker, unpublished, 2013
34 Changes in the numbers of postsynaptic densities in layer 3 cells during MD Espinosa & Stryker, unpublished, 2013
35 Changes in the numbers of postsynaptic densities in layer 3 cells during MD Espinosa & Stryker, unpublished, 2013
36 Ocular dominance of labeled cells in layer 3 measured by 2-photon calcium imaging Espinosa & Stryker, unpublished, 2013
37 Relationship between anatomical changes in the numbers of postsynaptic densities in single layer 3 cells after 3 days MD as a function of ocular dominance measured by 2-photon calcium imaging Espinosa & Stryker, unpublished, 2013
38 Changes in the intensities of persistent postsynaptic densities in layer 3 cells during MD Espinosa & Stryker, unpublished, 2013
39 Changes in the numbers of presynaptic boutons in layer 3 cells during MD Espinosa & Stryker, unpublished, 2013
40 Changes in the intensities of presynaptic boutons in layer 3 cells during MD Espinosa & Stryker, unpublished, 2013
41 What activity in primary visual cortex drives plasticity? The plasticity takes place only when mice are alert Adapted from Dombeck et al, 2007 Niell and Stryker, Neuron, 2010
42 Recording from Alert Mouse on a Stryofoam Ball Floating On Air Niell and Stryker, Neuron, 2010
43 Single unit responses in excitatory neurons Stationary Moving Niell and Stryker, Neuron, 2010
44 No change with locomotion in firing rate in LGN Niell and Stryker, Neuron, 2010
45 Ca ++ imaging in awake mouse confirms increased response with locomotion Locomotion Stationery Niell, 2010, unpublished
46 Locomotion specifically increases amplitude of visual responses in cortex, with no change in tuning or in spontaneous rate. Niell and Stryker, Neuron, 2010
47 Would these enhanced responses increase plasticity in adult visual cortex? Could this be the basis of effects of enriched environments, antidepressants, and many other manipulations reported to enhance plasticity? To test this idea we studied a mouse model of recovery from amblyopia.
48 Slow and incomplete recovery of closed-eye responses in adult V1 after prolonged MD Monocular visual deprivation for ~5 months beginning in critical period. Then open deprived eye and measure visual responses at weekly intervals using intrinsic signal imaging. Kaneko & Stryker elife 2014
49 Restoration of cortical responses in adult mouse after prolonged visual deprivation Monocular deprivation for ~5 months beginning in critical period. Open deprived eye and image visual responses at weekly intervals. Experimental treatment: Visual stimulation during locomotion Control treatments: Locomotion only (gray screen) Visual stimulation only (in home cage) Home cage ~4h/day ~4 h/day ~8h/day 24h/day Kaneko & Stryker elife 2014
50 Locomotion + visual stimulation enhances recovery of deprived-eye responses in visual cortex Days after re-opening closed eye Kaneko & Stryker elife 2014
51 Little effect of locomotion without visual stimulation or visual stimulation alone Kaneko & Stryker elife 2014
52 Kaneko & Stryker elife 2014
53 Kaneko & Stryker elife 2014
54 Enhancement of recovery by running is stimulus-specific Kaneko & Stryker elife 2014
55 Binocular matching of preferred orientation recovers well only in animals viewing grating stimuli during locomotion Kaneko & Stryker elife 2014
56 Responses of broad-spiking cells recover fully and specifically Kaneko & Stryker elife 2014
57 Responses of narrow-spiking cells show little recovery Kaneko & Stryker elife 2014
58 Spontaneous firing of narrow-spiking cells is tremendously reduced, and that of broad spiking cells increased Kaneko & Stryker elife 2014
59 What pathways enhance cortical activity with locomotion? ChR2 stimulation of a brainstem cholinergic nucleus, the pedunculopontine tegmental nucleus (PPTg) Cholinergic pathways PPTg Moses Lee (Wilbrecht lab)and Cris Niell, unpublished
60
61 Lower freq stimulation does not induce running but does induce gamma and visual response gain Moses Lee (Wilbrecht lab) and Cris Niell, unpublished
62 Optogenetic stimulation increases visual response gain Moses Lee (Wilbrecht lab) and Cris Niell, unpublished
63 ChR2 stimulation of PPTg: ascending connections mediate increase in visual response gain. Cholinergic pathways??? PPTg X Moses Lee (Wilbrecht lab) and Cris Niell, unpublished
64 ChR2 stimulation of PPTg: ascending connections mediate increase in visual response gain. Cholinergic pathways??? PPTg X Moses Lee (Wilbrecht lab) and Cris Niell, unpublished
65 ChR2 stimulation of PPTg afferents to basal forebrain partially mimics effect of locomotion on visual response gain. Moses Lee (Wilbrecht lab) and Cris Niell, unpublished
66 What is the cortical circuit for enhancing V1 activity by locomotion??? PPTg X
67 VIP inhibitory neurons shown in 2-photon microscopy VIP cell Non-VIP cell Fu et al Cell 2014
68 VIP neuron active during running in the dark Fu et al Cell 2014
69 How can activity in an inhibitory neuron enhance activity in the cortical circuit? Pfeffer et al., Nature, 2013
70 Somatostatin neuron becomes silent during locomotion in the dark fluorescence (ΔF/F%) Running Speed (cm/s) SST GCaMP6 Time (s) Fu et al Cell 2014
71 Where do the VIP neurons get their input? Fu et al Cell 2014
72 VIP neurons receive input from neurons in the Nucleus of the diagonal Band of Broca (NDDB) in the basal forebrain Fu et al Cell 2014
73 VIP neurons activated through nicotinic cholinergic receptors Fu et al Cell 2014
74 Activation of VIP neurons by locomotion involves nicotinic acetylcholine receptors Fu et al Cell 2014
75 Optogenetic Activation of VIP neurons enhances visual responses in V1 Fu et al Cell 2014
76 Photolytic Damage to VIP neurons blocks enhancement of visual responses in V1 Fu et al Cell 2014
77 The anatomical elements of the VIP cell circuit for enhancing gain in V1 are present in all rodent, carnivore and primate cortical areas that I have looked at. Cholinergic effects on learning and brain plasticity have also widely been reported, although the cortical portions of the neural circuits responsible have not been identified. We believe that the same circuit activated by locomotion in the mouse is likely to account for diverse phenomena of gain enhancement, such as focal attention in primates.
78 Megumi Kaneko: Mechanisms of plasticity Enhancement of adult plasticity by exercise and visual stimulation Megumi Cris Niell: Mouse receptive fields, Enhancement of responses by locomotion Optogenetic stimulation of locomotion in collaboration with Moses Lee, Linda Wilbrecht and Antonello Bonci J. Sebastian Espinosa: Anatomy in vivo Yu Fu: Cortical circuit for locomotion, with J.Tucciarone, J.S. Espinosa, Z. Josh Huang Cris Sebastian Yu Moses Support from NEI, NIMH, NINDS, UCPPFP & Helen Hay Whitney Foundation
79 (end of talk)
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