Abstract:A general theory views the function of all neurons as prediction, and one component of this theory is that of “predictive homeostasis” or “prediction error.” It is well established that sensory systems adapt so that neuronal output maintains sensitivity to sensory input, in accord with information theory. Predictive homeostasis applies the same principle at the cellular level, where the challenge is to maintain membrane excitability at the optimal homeostatic level so that spike generation is maximally sensiti… Show more
“…Burst and tonic response modes are often described as binary states, which is an accurate description for the extreme ends of behavioral arousal: tonic mode during active sensory processing and burst mode during sleep and anesthesia. This hard distinction, however, fails to capture thalamic processing during the transition between the two response modes (Deleuze et al, 2012;Hong et al, 2014). In between the extremes of focused sensory processing and slow-wave sleep, the graded deinactivation of the T-channels of a cell may play a previously underappreciated role in visual processing (Mease et al, 2017).…”
Section: Thalamic Burst Mode and Behavioral Statementioning
confidence: 99%
“…When this occurs, depolarizing stimuli can activate T-channels to generate a Ca 2ϩ potential (T-potential), which can then trigger a short train of high frequency, Na ϩ -based action potentials. It is important to note that the magnitude of the T-potential and subsequently the number of spikes it triggers depend on the percentage of T-channels in the deinactivated versus the inactivated state, which, in turn, depends on the depth and duration of the preceding hyperpolarization (Deschênes et al, 1984;Destexhe and Sejnowski, 2002;Hong et al, 2014).…”
Retinal signals are transmitted to cortex via neurons in the lateral geniculate nucleus (LGN), where they are processed in burst or tonic response mode. Burst mode occurs when LGN neurons are sufficiently hyperpolarized for T-type Ca 2ϩ channels to deinactivate, allowing them to open in response to depolarization, which can trigger a high-frequency sequence of Na ϩ-based spikes (i.e., burst). In contrast, T-type channels are inactivated during tonic mode and do not contribute to spiking. Although burst mode is commonly associated with sleep and the disruption of retinogeniculate communication, bursts can also be triggered by visual stimulation, thereby transforming the retinal signals relayed to the cortex. To determine how burst mode affects retinogeniculate communication, we made recordings from monosynaptically connected retinal ganglion cells and LGN neurons in male/female cats during visual stimulation. Our results reveal a robust augmentation of retinal signals within the LGN during burst mode. Specifically, retinal spikes were more effective and often triggered multiple LGN spikes during periods likely to have increased T-type Ca 2ϩ channel activity. Consistent with the biophysical properties of T-type Ca 2ϩ channels, analysis revealed that effect magnitude was correlated with the duration of the preceding thalamic interspike interval and occurred even in the absence of classically defined bursts. Importantly, the augmentation of geniculate responses to retinal input was not associated with a degradation of visual signals. Together, these results indicate a graded nature of response mode and suggest that, under certain conditions, bursts facilitate the transmission of visual information to the cortex by amplifying retinal signals.
“…Burst and tonic response modes are often described as binary states, which is an accurate description for the extreme ends of behavioral arousal: tonic mode during active sensory processing and burst mode during sleep and anesthesia. This hard distinction, however, fails to capture thalamic processing during the transition between the two response modes (Deleuze et al, 2012;Hong et al, 2014). In between the extremes of focused sensory processing and slow-wave sleep, the graded deinactivation of the T-channels of a cell may play a previously underappreciated role in visual processing (Mease et al, 2017).…”
Section: Thalamic Burst Mode and Behavioral Statementioning
confidence: 99%
“…When this occurs, depolarizing stimuli can activate T-channels to generate a Ca 2ϩ potential (T-potential), which can then trigger a short train of high frequency, Na ϩ -based action potentials. It is important to note that the magnitude of the T-potential and subsequently the number of spikes it triggers depend on the percentage of T-channels in the deinactivated versus the inactivated state, which, in turn, depends on the depth and duration of the preceding hyperpolarization (Deschênes et al, 1984;Destexhe and Sejnowski, 2002;Hong et al, 2014).…”
Retinal signals are transmitted to cortex via neurons in the lateral geniculate nucleus (LGN), where they are processed in burst or tonic response mode. Burst mode occurs when LGN neurons are sufficiently hyperpolarized for T-type Ca 2ϩ channels to deinactivate, allowing them to open in response to depolarization, which can trigger a high-frequency sequence of Na ϩ-based spikes (i.e., burst). In contrast, T-type channels are inactivated during tonic mode and do not contribute to spiking. Although burst mode is commonly associated with sleep and the disruption of retinogeniculate communication, bursts can also be triggered by visual stimulation, thereby transforming the retinal signals relayed to the cortex. To determine how burst mode affects retinogeniculate communication, we made recordings from monosynaptically connected retinal ganglion cells and LGN neurons in male/female cats during visual stimulation. Our results reveal a robust augmentation of retinal signals within the LGN during burst mode. Specifically, retinal spikes were more effective and often triggered multiple LGN spikes during periods likely to have increased T-type Ca 2ϩ channel activity. Consistent with the biophysical properties of T-type Ca 2ϩ channels, analysis revealed that effect magnitude was correlated with the duration of the preceding thalamic interspike interval and occurred even in the absence of classically defined bursts. Importantly, the augmentation of geniculate responses to retinal input was not associated with a degradation of visual signals. Together, these results indicate a graded nature of response mode and suggest that, under certain conditions, bursts facilitate the transmission of visual information to the cortex by amplifying retinal signals.
“…The theory should predict the properties of voltage-gated ion channels as it did IPSG. For example, the theory correctly predicted the experimental observation that T-type calcium channels are homoeostatic in counterbalancing opponent IPSG in thalamocortical neurons of LGN50. The more general theory proposes differences between sensory and motor neurons, and it correctly predicted evidence that T-type calcium channels are not homoeostatic but cause bursts of spikes in motor thalamus51.…”
Synaptic inhibition counterbalances excitation, but it is not known what constitutes optimal inhibition. We previously proposed that perfect balance is achieved when the peak of an excitatory postsynaptic potential (EPSP) is exactly at spike threshold, so that the slightest variation in excitation determines whether a spike is generated. Using simulations, we show that the optimal inhibitory postsynaptic conductance (IPSG) increases in amplitude and decay rate as synaptic excitation increases from 1 to 800 Hz. As further proposed by theory, we show that optimal IPSG parameters can be learned through anti-Hebbian rules. Finally, we compare our theoretical optima to published experimental data from 21 types of neurons, in which rates of synaptic excitation and IPSG decay times vary by factors of about 100 (5-600 Hz) and 50 (1-50 ms), respectively. From an infinite range of possible decay times, theory predicted experimental decay times within less than a factor of 2. Across a distinct set of 15 types of neuron recorded in vivo, theory predicted the amplitude of synaptic inhibition within a factor of 1.7. Thus, the theory can explain biophysical quantities from first principles.
“…We previously tested this by examining the function of T-type calcium channel (TtCC) in thalamocortical (TC) neurons of the lateral geniculate nucleus (LGN) while mimicking natural conditions. We found that TtCC amplified EPSPs toward spike threshold so that EPSPs may or may not cause spikes, depending on their amplitude ( Hong et al, 2014 ). This supports our theory, according to which TtCC in sensory neurons should help to maximize the causal link between synaptic excitation and spikes without themselves causing spikes, through a process we have termed “predictive homeostasis” ( Fiorillo et al, 2014 ; Hong et al, 2014 ).…”
Section: Introductionmentioning
confidence: 99%
“…We found that TtCC amplified EPSPs toward spike threshold so that EPSPs may or may not cause spikes, depending on their amplitude ( Hong et al, 2014 ). This supports our theory, according to which TtCC in sensory neurons should help to maximize the causal link between synaptic excitation and spikes without themselves causing spikes, through a process we have termed “predictive homeostasis” ( Fiorillo et al, 2014 ; Hong et al, 2014 ). In this model of a sensory neuron, TtCC are one of many voltage-gated ion channel (VGC) subtypes predicting and counteracting sensory-related synaptic drive so that each spike signals a positive prediction error, in the spirit of “predictive coding” (e.g., Barlow, 1961 ).…”
Although neurons within intact nervous systems can be classified as ‘sensory’ or ‘motor,’ it is not known whether there is any general distinction between sensory and motor neurons at the cellular or molecular levels. Here, we extend and test a theory according to which activation of certain subtypes of voltage-gated ion channel (VGC) generate patterns of spikes in neurons of motor systems, whereas VGC are proposed to counteract patterns in sensory neurons. We previously reported experimental evidence for the theory from visual thalamus, where we found that T-type calcium channels (TtCCs) did not cause bursts of spikes but instead served the function of ‘predictive homeostasis’ to maximize the causal and informational link between retinogeniculate excitation and spike output. Here, we have recorded neurons in brain slices from eight sensory and motor regions of rat thalamus while mimicking key features of natural excitatory and inhibitory post-synaptic potentials. As predicted by theory, TtCC did cause bursts of spikes in motor thalamus. TtCC-mediated responses in motor thalamus were activated at more hyperpolarized potentials and caused larger depolarizations with more spikes than in visual and auditory thalamus. Somatosensory thalamus is known to be more closely connected to motor regions relative to auditory and visual thalamus, and likewise the strength of its TtCC responses was intermediate between these regions and motor thalamus. We also observed lower input resistance, as well as limited evidence of stronger hyperpolarization-induced (‘H-type’) depolarization, in nuclei closer to motor output. These findings support our theory of a specific difference between sensory and motor neurons at the cellular level.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.