Timing and Specificity of Feed-Forward Inhibition within the LGN

Blitz, Dawn M.; Regehr, Wade G.

doi:10.1016/j.neuron.2005.01.033

Cited by 132 publications

(198 citation statements)

References 59 publications

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“…The temporal window established between the onset of excitation and the peak of inhibition closely agreed with the excitatory PSP width and the duration of suprathreshold responses observed in spiking neurons, suggesting that the timing of spike output in L4 is a direct consequence of the dynamic interaction between excitatory and inhibitory inputs. A similar sequence of excitation followed by inhibition also plays a role in shaping spike timing in the auditory cortex (Wehr and Zador, 2003), hippocampus (Pouille and Scanziani, 2001), cerebellum (Mittmann et al, 2005), and thalamus (Blitz and Regehr, 2005). Our present findings, combined with this accumulated Figure 5.…”

Section: Discussionsupporting

confidence: 76%

“…In the rodent whisker system, ascending thalamic input engages neuronal circuits in cortical layer 4 (L4), consisting of excitatory spiny stellate and pyramidal cells as well as aspiny interneurons (White and Rock, 1981;Beierlein et al, 2002Beierlein et al, , 2003Bruno and Simons, 2002) that provide feedforward and feedback inhibition to the local network (Agmon and Connors, 1991;Swadlow and Gusev, 2000;Porter et al, 2001;Swadlow, 2003;Staiger et al, 2004). This functional architecture leads to a precise sequence of excitation followed by inhibition in response to whisker deflection that may serve to sharpen the spike timing of suprathreshold responses and limit the time for integration of excitatory inputs (Pinto et al, 2000(Pinto et al, , 2003Pouille and Scanziani, 2001;Wehr and Zador, 2003;Wilent and Contreras, 2004;Blitz and Regehr, 2005;Mittmann et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

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Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation

Higley¹,

Contreras²

2006

J. Neurosci.

252

244

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In layer 4 (L4) of the rat barrel cortex, a single whisker deflection evokes a stereotyped sequence of excitation followed by inhibition, hypothesized to result in a narrow temporal window for spike output. However, awake rats sweep their whiskers across objects, activating the cortex at frequencies known to induce short-term depression at both excitatory and inhibitory synapses within L4. Although periodic whisker deflection causes a frequency-dependent reduction of the cortical response magnitude, whether this adaptation involves changes in the relative balance of excitation and inhibition and how these changes might impact the proposed narrow window of spike timing in L4 is unknown. Here, we demonstrate for the first time that spike output in L4 is determined precisely by the dynamic interaction of excitatory and inhibitory conductances. Furthermore, we show that periodic whisker deflection results in balanced adaptation of the magnitude and timing of excitatory and inhibitory input to L4 neurons. This balanced adaptation mediates a reduction in spike output while preserving the narrow time window of spike generation, suggesting that L4 circuits are calibrated to maintain relative levels of excitation and inhibition across varying magnitudes of input.

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Section: Discussionsupporting

confidence: 76%

Section: Introductionmentioning

confidence: 99%

Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation

Higley¹,

Contreras²

2006

J. Neurosci.

252

244

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“…In contrast, we propose that such shifts are not encoding variables; instead, they have a structural role in maintaining response density across a wide range of input conditions. The existence of comparable feedforward inhibitory pathways in a number of neural circuits, including hippocampus 11,32 , cerebellum 12,27 , lateral geniculate nucleus 33 and sensory circuits sensitive to the precise timing of excitatory input 6,34 , suggests the potentially widespread applicability of the mechanism described here.…”

Section: Discussionmentioning

confidence: 87%

Adaptive regulation of sparseness by feedforward inhibition

et al. 2007

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In the mushroom body of insects, odors are represented by very few spikes in a small number of neurons, a highly efficient strategy known as sparse coding. Physiological studies of these neurons have shown that sparseness is maintained across thousand-fold changes in odor concentration. Using a realistic computational model, we propose that sparseness in the olfactory system is regulated by adaptive feedforward inhibition. When odor concentration changes, feedforward inhibition modulates the duration of the temporal window over which the mushroom body neurons may integrate excitatory presynaptic input. This simple adaptive mechanism could maintain the sparseness of sensory representations across wide ranges of stimulus conditions. Our sensory environment is in near constant flux. Brain sensory systems have evolved the means to adjust their coding properties to adapt to constantly changing signals arising in sensory neurons. Ideally, a coding strategy used by a sensory system should provide efficient representations across the full possible range of stimulation conditions. For the olfactory system, this task involves the encoding of odor intensities, an ability that is critical in many species for survival. Psychophysics studies have shown that, across great ranges of concentrations, odors can be perceived as arising from the same chemical 1,2 , and yet, human and animal subjects can distinguish their concentrations as well. Odor representations in the olfactory system have been shown to remain sparse and specific over thousand-fold changes in odor concentration 3 , a property that is potentially useful for storing and retrieving memories [4][5][6] . Given these variations in input, the method by which neural circuits of the olfactory system regulate sensory input to maintain stable odor representations remains a mystery.

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“…Furthermore, given that the concentration of ambient GABA in vivo is likely to depend on the activity of GABA-releasing neurons, we might expect that tonic current amplitude would dynamically fluctuate. Thus, under conditions in which GABA-releasing neurons are more excited (Steriade et al, 1993;Blitz and Regehr, 2005;Steriade, 2005), not only synaptic inhibition but also tonic inhibition in TC neurons may be enhanced.…”

Section: Properties Of the Tonic Gaba A Currentmentioning

confidence: 99%

“…We also tested whether GABAergic neurons of the nucleus reticularis thalami (NRT), which do not express ␣4 and ␦ subunits (Wisden et al, 1992;Pirker et al, 2000), exhibit tonic inhibition. Determining the presence of tonic inhibition in thalamic neurons is of importance because GABA A receptors are an integral component of physiological (Steriade et al, 1993;Blitz and Regehr, 2005) and pathophysiological (Slaght et al, 2002;Steriade, 2005) thalamic mechanisms.…”

Section: Introductionmentioning

confidence: 99%

GABA_AReceptor-Mediated Tonic Inhibition in Thalamic Neurons

Cope

Hughes²,

Crunelli³

2005

J. Neurosci.

284

342

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Tonic GABA A receptor-mediated inhibition is typically generated by ␦ subunit-containing extrasynaptic receptors. Because the ␦ subunit is highly expressed in the thalamus, we tested whether thalamocortical (TC) neurons of the dorsal lateral geniculate nucleus (dLGN) and ventrobasal complex exhibit tonic inhibition. Focal application of gabazine (GBZ) (50 M) revealed the presence of a 20 pA tonic current in 75 and 63% of TC neurons from both nuclei, respectively. No tonic current was observed in GABAergic neurons of the nucleus reticularis thalami (NRT). Bath application of 1 M GABA increased tonic current amplitude to ϳ70 pA in 100% of TC neurons, but it was still not observed in NRT neurons. In dLGN TC neurons, the tonic current was sensitive to low concentrations of the ␦ subunit-specific receptor agonists allotetrahydrodeoxycorticosterone (100 nM) and 4,5,6,7-tetrahydroisoxazolo[5,4-c]-pyridin-3-ol (THIP) (100 nM) but insensitive to the benzodiazepine flurazepam (5 M). Bath application of low concentrations of GBZ (25-200 nM) preferentially blocked the tonic current, whereas phasic synaptic inhibition was primarily maintained. Under intracellular current-clamp conditions, the preferential block of the tonic current with GBZ led to a small depolarization and increase in input resistance. Using extracellular single-unit recordings, block of the tonic current caused the cessation of low-threshold burst firing and promoted tonic firing. Enhancement of the tonic current by THIP hyperpolarized TC neurons and promoted burst firing. Thus, tonic current in TC neurons generates an inhibitory tone. Its modulation contributes to the shift between different firing modes, promotes the transition between different behavioral states, and predisposes to absence seizures.

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Timing and Specificity of Feed-Forward Inhibition within the LGN

Cited by 132 publications

References 59 publications

Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation

Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation

Adaptive regulation of sparseness by feedforward inhibition

GABA_AReceptor-Mediated Tonic Inhibition in Thalamic Neurons

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Timing and Specificity of Feed-Forward Inhibition within the LGN

Cited by 132 publications

References 59 publications

Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation

Balanced Excitation and Inhibition Determine Spike Timing during Frequency Adaptation

Adaptive regulation of sparseness by feedforward inhibition

GABAAReceptor-Mediated Tonic Inhibition in Thalamic Neurons

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Resources

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GABA_AReceptor-Mediated Tonic Inhibition in Thalamic Neurons