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The Journal of Neuroscience, July 30, 2003, 23(17):6695-6702
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Rapid Critical Period Induction by Tonic Inhibition in Visual Cortex
Youichi Iwai,1 Michela Fagiolini,1 Kunihiko Obata,2 andTakao K. Hensch1 1Laboratory for Neuronal Circuit Development, The Institute of Physical and Chemical Research (RIKEN) Brain Science Institute, Saitama 351-0198, Japan, and 2Laboratory for Neurochemistry, National Institute for Physiological Sciences, Myodaiji, Okazaki 444-8585 Japan
Abstract
Top
Abstract
Introduction
Mice lacking a synaptic isoform of glutamic acid decarboxylase (GAD65) do not exhibit ocular dominance plasticity unless an appropriate level of GABAergic transmission is restored by direct infusion of benzodiazepines into the brain. To better understand how intracortical inhibition triggers experience-dependent changes, we dissected the precise timing requirement for GABA function in the monocular deprivation (MD) paradigm.Diazepam (DZ) or vehicle solution was infused daily before and/or during 4 d of MD in GAD65 knock-out mice. Extracellular single-unit recordings from the binocular zone of visual cortex were performed at the end of deprivation. We found that a minimum treatment of 2 d near the beginning of MD was sufficient to fully activate plasticity but did not need to overlap the deprivation per se. Extended delay after DZ infusion eventually led to loss of plasticity accompanied by improved intrinsic inhibitory circuit function. Two day DZ treatment just after eye opening similarly closed the critical period prematurely in wild-type mice.
Raising wild-type mice in complete darkness from birth delayed the peak sensitivity to MD as in other mammals. Interestingly, 2 d DZ infusion in the dark also closed the critical period, whereas equally brief light exposure during dark-rearing had no such effect. Thus, enhanced tonic signaling through GABAA receptors rapidly creates a milieu for plasticity within neocortex capable of triggering a critical period for ocular dominance independent of visual experience itself.
Key words: GAD65; dark-rearing; GABA; diazepam; critical period; visual cortex
Introduction
The mammalian brain is shaped by experience during restricted "critical periods" in early life. Even briefly occluding one eye during this time causes a prominent shift of responsiveness [ocular dominance (OD)] in favor of the open eye in primary visual cortex. Monocular deprivation (MD) fails to induce significant changes later in adulthood, indicating an irreversible developmental process defines the transient sensitivity to MD. Typically plasticity is absent at eye opening, peaks at4 weeks, and gradually declines over weeks (rodents: Fagiolini et al., 1994
; Gordon and Stryker, 1996
Focus on cortical inhibition has recently provided major cellular insight into the critical period. Mice lacking a synaptic isoform of GABA-synthetic enzyme glutamic acid decarboxylase [GAD65 knock-out (KO) mice] exhibit reduced cortical GABA release with stimulation and do not respond to brief MD (Hensch et al., 1998
These findings suggest that an evolving inhibitory-excitatory balance within cortex underlies the relatively late onset of the normal critical period. Direct enhancement of GABAergic transmission with diazepam prematurely reveals OD plasticity in young WT mice before their natural plastic period (Fagiolini and Hensch, 2000
To better understand how inhibition induces plasticity in vivo, we determined the timing requirement for GABAergic transmission using the GAD65 KO mouse model and systematically varying the period of diazepam exposure before and/or during a saturating 4 d MD. We found an initial 2 d infusion to be sufficient for full OD shifts that strikingly did not need to overlap the time of deprivation itself. Moreover, brief infusion eventually closed the critical period in correlation with improved cortical inhibition not only in KO mice, but also in WT animals raised in complete darkness. Our findings reveal that tonic GABAA-mediated signaling (independent of phasic, visual input) rapidly triggers lasting cellular refinements that direct OD plasticity in visual cortex.
Materials and Methods
Animals. Mice carrying a functional disruption of GAD65 were generated as described previously (Asada et al., 1996
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Figure 1. Brief DZ infusion is sufficient to rescue MD effects in GAD65 KO mice. A, OD histogram of nondeprived GAD65 KO mice exhibits a typical contralateral (cont.) eye bias. Number of animals and cells as indicated. B, DZ infusion the day before and on the first day of a 4 d MD shift OD toward the open, ipsilateral (ipsi.) eye in GAD65 KO mice, yielding a balanced distribution (p < 0.0001 vs no MD; 2 test). C, D, WT mice during the critical period (C) and GAD65 KO mice infused for 5 d (D) display similar OD distributions in response to 4 d MD. Neither is significantly different from that in B (p > 0.2 and p > 0.08, respectively;
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Figure 2. Initial 2 d DZ treatment at MD onset is minimum effective requirement. A, Each symbol represents CBI per animal. Filled and open symbols indicate GAD65 KO and WT mice, respectively. Whereas DZ infusion just the day before 4 d MD (Pre 1d) slightly reduces the CBI (0.63 ± 0.04; p > 0.08 vs no MD; t test), a further 1, 2, or 4 d of treatment into brief MD shifts the OD to a similarly significant extent (0.55 ± 0.03, 0.54 ± 0.02, 0.51 ± 0.03 for first 2 d, 3 d, full 5 d, respectively; p < 0.002 vs no MD; t test). These values are identical to WT mice deprived during the critical period (0.54 ± 0.01; p > 0.4; t test). B, DZ infusion for the last 2 d during a 4 d MD (Last 2 d) is ineffective (0.66 ± 0.02, n = 5; p < 0.04 vs first 2 d DZ; t test). Shaded region indicates range of nondeprived CBIs for GAD65 KO mice. *p < 0.05, **p < 0.01, t test.
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Figure 3. Two day DZ pretreatment produces a plastic milieu independent of MD. A, Vehicle or DZ infusion for 2 d was completed 1 d before brief MD in GAD65 KO mice (Pre 2d Veh; Pre 2d DZ). B, Pre 2d DZ induces a significant reduction of CBI values (0.48 ± 0.03, n = 6 vs 0.71 ± 0.02, n = 3 for Pre 2d Veh; p < 0.003; t test). C, D, GAD65 KO mice with Pre 2d DZ (D) exhibit prominent OD shifts toward the open, ipsilateral eye [p < 0.0001 vs Pre 2d Veh (C);
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Figure 6. Brief DZ prematurely closes, and DR delays critical period onset in WT mice. A-C, MD 10 d after 2 d of DZ infusion at P16 (A, P16 DZ + 10d) produces little or no ocular dominance shift, compared with MD during the same period without pretreatment (B, P28 LR; p < 0.002,
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Figure 7. Brief DZ (but not light exposure) closes the critical period during DR in WT mice. A, WT mice reared in complete darkness from birth, except for 2-4 d light exposure at P30, underwent MD as adults (>P50). B, Whereas WT mice reared normally hardly respond to brief MD in adulthood (Adult+MD, CBI = 0.69 ± 0.02; n = 3), DR mice shift significantly (Adult DR+MD, CBI = 0.57 ± 0.03; n = 9; p < 0.03 vs Adult+MD; t test). Light exposure for 2-4 d during DR has little effect on the delayed OD plasticity (2d light+MD, CBI = 0.60 ± 0.02; n = 9; p < 0.03 vs Adult+MD; t test). C, Vehicle (Veh) or DZ-treated (2 d at P30) DR mice were later subjected to MD as adults (>P50). D, DZ pretreatment in the dark eliminates the typical delay of OD plasticity (2d DZ+MD, CBI = 0.71 ± 0.01; n = 8), whereas vehicle infusion does not (2d Veh+MD, 0.61 ± 0.02, n = 6, p < 0.004 vs 2d DZ+MD; t test; Welch's correction). Shaded region indicates range of nondeprived CBIs for DR mice (0.75 ± 0.02; n = 6) that was significantly different from that of DR+MD, 2d light+MD, or 2d Veh+MD (p < 0.001) but not from Adult+MD or 2d DZ+MD (p > 0.09). **p < 0.03.
Monocular deprivation and drug infusion. MD and drug infusion were performed as described previously (Hensch et al., 1998
Electrophysiological recording and analysis. Surgical and electrophysiological procedures were as described in detail elsewhere (Gordon and Stryker, 1996
Results
Two day diazepam treatment fully rescues plasticity in GAD65 KO mice
Postsynaptic enhancement of GABAergic transmission by DZ concurrent with brief MD can completely restore OD plasticity to mice whose GABA release is functionally compromised. Both local cortical infusion through an osmotic minipump system and global treatment by repeated intraventricular injection are similarly effective (Hensch et al., 1998We performed extracellular single-unit recordings in the binocular zone of primary visual cortex, and evaluated every cell on a seven-point OD scale (see Materials and Methods) (Daw, 1995
When intraventricular DZ injections were initiated the day before and continued throughout a brief 4 d period of MD, a prominent shift of OD in favor of the open eye was produced, confirming earlier results from an independent line of GAD65 KO mice (Hensch et al., 1998
Further shortening DZ infusion for just the initial 2 d, 1 d before and the first day of MD, still produced a significant OD shift (Fig. 1B) (p < 0.0001 vs No MD;
On the other hand, DZ treatment during the latter half of MD was ineffective. Little OD plasticity was observed in GAD65 KO mice infused only during the last 2 d of MD (Fig. 2B)(p > 0.1 vs no MD; p < 0.04 vs first 2 d DZ + MD; t test). GABA circuits must, therefore, play a critical role in starting experience-dependent changes that are eventually consolidated by other factors.
Brief diazepam exposure triggers a limited sensitive period for MD
Whereas initial 2 d infusion had a prominent effect on OD shifts, preinjection of DZ just the day before MD yielded only slight, variable plasticity (Fig. 2A) (p > 0.08 vs no MD; t test). This suggests that optimal GABAergic transmission during the first day of MD may be critical for full OD plasticity. An appropriate inhibitory-excitatory balance may actively detect perturbations in sensory input from the two eyes. Alternatively, pretreatment might effectively establish a plastic environment over a 2 d period because OD did shift in some cases with just 1 d of preinfusion (Fig. 2A).To distinguish between these possibilities, brief MD for 4 d was started 1 d after 2 d of DZ treatment (Fig. 3A, Pre 2d DZ). This insured that the drug had washed out completely before MD (Berrueta et al., 1992
Thus, 2 d DZ treatment is the minimum requirement for full OD plasticity to occur in GAD65 KO mice and need not overlap the time of monocular occlusion. We then explored whether this sensitivity to MD is eventually lost, as occurs normally in WT animals. Previously, it was shown that GAD65 KO mice retain the potential for OD plasticity throughout life, because both brief MD concurrent with DZ and long-term MD alone produce significant shifts even at adult stages (Fagiolini and Hensch, 2000
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Figure 4. Early 2 d DZ treatment abolishes adult plasticity in GAD65 KO mice. A, GAD65 KO mice were preinfused with DZ or vehicle for 2 d, followed 14 or >60 d later by 4 d MD concurrent with DZ infusion. B, Whereas vehicle infusion leaves the mutant sensitive to MD into adulthood even 60 d later (Veh + 60d, CBI = 0.58 ± 0.01; n = 3), DZ pretreatment abolishes this plastic potential (DZ + 60d, CBI = 0.71 ± 0.02, n = 3, p < 0.01 vs Veh + 60d; t test), identical to that of nondeprived adult mice (no MD, CBI = 0.70 ± 0.02; n = 4). Just 14 d after DZ treatment, plasticity partially remains (DZ + 14d, CBI = 0.61 ± 0.01, n= 3, p < 0.03 vs DZ + 60d, t test) but is already significantly reduced compared with the maximal shift at 1 d after DZ (p < 0.03 vs DZ + 1d; t test). *p < 0.05, **p < 0.01, t test.
However, when DZ was infused for 2 d around P30, 2 months later (at P90) neither 4 d MD concurrent with 5 d DZ treatment (Fig. 4) (p > 0.7 vs adult no MD; t test) nor long-term MD (p > 0.4 vs adult no MD; t test) produced any OD shift. An intermediate time interval of 2 weeks after brief DZ infusion still showed a residual plasticity that was, however, significantly weaker than the maximal shift induced shortly after drug treatment. Two day DZ exposure in GAD65 KO mice is, therefore, sufficient to gradually eliminate sensitivity to MD with a time course similar to the natural critical period in mice (Gordon and Stryker, 1996
Brief diazepam triggers progressive maturation of intracortical inhibition
Whereas OD shifts were induced immediately after brief DZ treatment, this plasticity was abolished later, suggesting that DZ triggered irreversible changes of intracortical circuitry to limit the plastic period. To address the cellular basis of this effect, we examined neuronal spiking behavior after visual stimulation. Prolonged discharge is an hyperexcitability of a single neuron when light-bar stimuli exit the receptive field of the cell (Hensch et al., 1998
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Figure 5. Brief DZ treatment progressively reduces prolonged discharge in GAD65 KO. A, Examples of neuronal responses showing normal (top trace) or prolonged discharge (bottom trace). Excess spikes in bottom trace continue even after light-bar stimuli have exited the receptive field (RF). B, Visual cortical neurons in GAD65 KO mice exhibit prolonged discharge throughout life (
We infused DZ for 2 d into GAD65 KO mice and waited for several periods before counting the proportion of neurons displaying prolonged discharge. Immediately after treatment, prolonged discharge was slightly but significantly reduced (Fig. 5B) (p < 0.03 vs no DZ; t test) consistent with the acute action of DZ on postsynaptic responses at active GABAergic synapses (Sieghart, 1995
Thus, once enhanced, GABAergic transmission had long-lasting effects on itself even after DZ was removed, triggering a progressive functional maturation of inhibitory circuits in parallel with the loss of plasticity. To examine such durable effects of 2 d DZ treatment even in WT animals, we infused young precritical period mice at P16 and recorded the response to MD 10 d later at the usual peak of plasticity. The OD shift was greatly attenuated and significantly different from normally reared animals deprived at this age (Fig. 6A,B) (p < 0.002;
Brief diazepam closes the critical period in dark-reared WT mice
Sensory input is believed to be essential for the functional refinement of neuronal circuits in the mammalian visual system. We thus examined whether the action of DZ depends on visual experience using WT animals. DR from birth maintains the visual cortex in an immature state, prolonging sensitivity to MD into adulthood (Cynader, 1983In other words, the onset of the critical period is delayed by DR. To first confirm this concept in mice, we recorded the response to MD after brief DR just to the usual peak of plasticity (Fig. 6C). Little or no OD shift was observed in comparison with light-reared controls at this age (Fig. 6B,D). In contrast, adult animals raised with normal visual experience exhibited little or no OD plasticity, whereas mice reared in complete darkness to adulthood (>P55) clearly retained this plastic capacity (Fig. 7B) (Fagiolini et al., 2003
In cat visual cortex, very brief visual experience (6 hr) during DR is reported to trigger a developmental process that eventually eliminates OD plasticity (Mower et al., 1983
In comparison, we injected DZ for 2 d into DR mice at approximately P30. A total of 20 min in the light under a dissecting microscope was required to complete these injections into mice anesthetized in the darkroom. This amount of light exposure is negligible given that several days were ineffective (Fig. 7B) and that plasticity mechanisms are precluded under anesthesia (Imamura and Kasamatsu, 1991
Remarkably, OD shifts could not be detected by MD in DR adult mice previously exposed to DZ (Fig. 7D) (p > 0.09 vs DR no MD; t test). As expected, vehicle treatment under the same conditions did not abolish the plasticity delayed by DR (Fig. 7B,D) (p < 0.001 vs DR no MD, p < 0.004 vs DR 2d DZ, t test). Moreover, the CBI for DR 2d DZ + MD was identical to that of light-reared adults + MD (p > 0.2; t test). Thus, 2 d DZ treatment eventually closes the critical period in complete darkness, replacing even longer periods of normal visual experience.
This supports the above results from GAD65 KO mice (Figs. 3, 4) suggesting that brief enhancement of inhibition may potently induce a plastic milieu independent of the sensory deprivation itself, which runs its course within 20 d after the treatment. In DR adult WT mice, a much lower proportion of prolonged discharge (23 ± 2%, 321 cells, 13 mice) was observed than in adult GAD65 mutants. Thus, DR produces a more subtle alteration of inhibition than the uniform reduction of GABA release caused by GAD65 deletion (Tsumoto and Freeman, 1987
Discussion
Our parametric study has demonstrated that brief DZ infusion can trigger a "critical period" independent of visual experience in developing neocortex. Moreover, the consequences far outlast the initial exposure, because MD is effective even without the continued presence of drug. The switch is thrown rapidly within 24-48 hr, and thus does not reflect a chronic response to drug treatment, such as withdrawal or tolerance after several days at high dose (Gallager et al., 1984Critical period activation by brief enhancement of inhibition
We have briefly manipulated two conditions under which the onset of OD plasticity is delayed. Mice lacking GAD65 harbor plasticity machinery that lies dormant throughout life unless an appropriate level of GABAergic transmission is exogenously supplied. Dark-reared mice similarly fail to activate plasticity with a normal time course. A common misconception about DR is that critical period onset is normal but then prolonged in duration. Both the evidence from cats (Mower, 1991One reason for the misconception about the effects of DR is the finding that orientation preference emerges even in the absence of visual experience (Crair et al., 1998
How can transiently enhanced GABAergic transmission replace visual experience to trigger the critical period for OD? Homeostatic mechanisms in the dark would act to reduce miniature IPSC amplitudes by decreasing the number of postsynaptic GABAA receptors clustered at neocortical synapses because of activity deprivation (Kilman et al., 2002
We propose a testable two-step process of inhibitory circuit refinement after DZ treatment as a basis for further study. Initially, acute benzodiazepine action may potentiate GABAergic transmission at individual synapses. Brief, augmented stimulation triggers long-term potentiation of inhibitory transmission in visual cortex that is induced postsynaptically (Komatsu, 1994
In the second stage, morphological changes may reinforce and stabilize relevant inhibitory connections. Formation of novel GABA synapses occurs with as little as 24 hr of whisker stimulation in barrel cortex (Knott et al., 2002
Specific GABA circuits may control critical period plasticity
The diverse array of neocortical interneurons is in fact precisely organized with respect to domains of synaptic contact onto target cells (Somogyi et al., 1998Central neurons receive a continuous barrage of GABAergic input (Mody, 2001
Actively released GABA acting on postsynaptic GABAA receptors is believed to mediate "phasic" inhibition, whereas "tonic" currents also result from the persistent activation of extrasynaptic receptors by ambient GABA. In granule cells of hippocampus and cerebellum, the latter contain
4 or
Tonic inhibitory input increases the electrotonic length of the dendritic tree and consequently increases attenuation of dendritic inputs as they propagate into the soma and axon (Hausser and Clark, 1997
Footnotes
Received Dec. 16, 2002; revised Apr. 29, 2003; accepted May. 30, 2003.This work was supported in part by the Special Postdoctoral Researchers Program at The Institute of Physical and Chemical Research (RIKEN) (Y.I.) and Special Coordination Funds for Promoting Science and Technology from Japan Science and Technology Corporation (T.K.H.). We thank S. Fujishima and Y. Mizuguchi for genotyping and maintenance of the GAD65 KO mouse colony.
Correspondence should be addressed to Takao Kurt Hensch, Laboratory for Neuronal Circuit Development, The Institute of Physical and Chemical Research (RIKEN) Brain Science Institute, 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan. E-mail: hensch{at}postman.riken.go.jp.
Copyright © 2003 Society for Neuroscience 0270-6474/03/236695-08$15.00/0
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