Neocortex saves energy by reducing coding precision during food scarcity

Padamsey, Zahid; Katsanevaki, Danai; Dupuy, Nathalie; Rochefort, Nathalie L.

doi:10.1016/j.neuron.2021.10.024

Cited by 64 publications

(95 citation statements)

References 93 publications

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“…We predict that, for visual sensory systems, a way to implement this solution might be to generally broaden the tuning curves of neurons responsive to oriented edges across the sensory space. The reason for postulating this quantifiable prediction is that adaptive broadening of orientation tuning is related to AMPA receptor conductance decrease, which, in turn, reduces synaptic ATP use, and should directly affect sensory discrimination performance ( 73 ). Experiments of this sort should help establish the link and quantify the balance between efficiency in adaptive information processing and metabolic consumption costs, which is crucial to promote reward maximization of the organism via goal-directed behavior.…”

Section: Discussionmentioning

confidence: 99%

Rational inattention in mice

et al. 2022

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Behavior exhibited by humans and other organisms is generally inconsistent and biased and, thus, is often labeled irrational. However, the origins of this seemingly suboptimal behavior remain elusive. We developed a behavioral task and normative framework to reveal how organisms should allocate their limited processing resources such that sensory precision and its related metabolic investment are balanced to guarantee maximal utility. We found that mice act as rational inattentive agents by adaptively allocating their sensory resources in a way that maximizes reward consumption in previously unexperienced stimulus-reward association environments. Unexpectedly, perception of commonly occurring stimuli was relatively imprecise; however, this apparent statistical fallacy implies “awareness” and efficient adaptation to their neurocognitive limitations. Arousal systems carry reward distribution information of sensory signals, and distributional reinforcement learning mechanisms regulate sensory precision via top-down normalization. These findings reveal how organisms efficiently perceive and adapt to previously unexperienced environmental contexts within the constraints imposed by neurobiology.

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Section: Discussionmentioning

confidence: 99%

Rational inattention in mice

et al. 2022

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“…Thus, the functional output of LH GABA neurons to disinhibit dopamine neurons is likely preserved in fasting leading to behavioural activation. An alternative hypothesis is that suppressed firing activity of tVTA/RMTg GABA neurons during fasting could be a mechanism associated with brain energy conservation during food scarcity, as has been observed in the neocortex which allowed for the significant conservation of ATP (Padamsey et al., 2021). However, as in Padamsey et al., 2021, synaptic functioning is preserved and activation of LH GABAergic inputs to tVTA/RMTg GABAergic neurons can override this fasting‐induced suppression of synaptic strength.…”

Section: Discussionmentioning

confidence: 99%

Activation of LH GABAergic inputs counteracts fasting‐induced changes in tVTA/RMTG neurons

Godfrey

Qiao

Borgland

2022

The Journal of Physiology

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“…Thus, the functional output of LH GABA neurons to disinhibit dopamine neurons is likely preserved in fasting leading to behavioural activation. An alternative hypothesis is that suppressed firing activity of tVTA/RMTg GABA neurons during fasting could be a mechanism associated with brain energy conservation during food scarcity, as has been observed in the neocortex which allowed for the significant conservation of ATP (Padamsey et al ., 2021). However, as in Padamsey et al ., 2021, synaptic functioning is preserved and activation of LH GABAergic inputs to tVTA/RMTg GABAergic neurons can override this fasting-induced suppression of synaptic strength.…”

Section: Discussionmentioning

confidence: 99%

Activation of LH GABAergic inputs counteracts fasting-induced changes in tVTA/RMTG neurons

Godfrey

Qiao

Borgland

2021

Preprint

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Dopamine neurons in the ventral tegmental area (VTA) are strongly innervated by GABAergic neurons in the ‘tail of the VTA’ (tVTA), also known as the rostralmedial tegmental nucleus (RMTg). Disinhibition of dopamine neurons through firing of the GABAergic neurons projecting from the lateral hypothalamus (LH) leads to reward seeking and consumption through dopamine release in the nucleus accumbens. VTA dopamine neurons respond to changes in motivational state, yet less is known of whether tVTA/RMTg GABAergic neurons or the LH GABAergic neurons that project to them are also affected by changes in motivational state, such as fasting. An acute 16 h overnight fast decreased the excitability of tVTA/RMTg GABAergic neurons of male and female mice. In addition, fasting decreased synaptic strength at LH GABA to tVTA/RMTg GABAergic synapses, indicated by reduced amplitude of optically evoked currents, decreased readily releasable pool (RRP) size and replenishment. Optical stimulation of LH GABA terminals suppressed evoked action potentials of tVTA/RMTg GABAergic neurons in unfasted mice, but this effect decreased following fasting in both males and females. Furthermore, during fasting, LH GABA inputs to tVTA/RMTg neurons maintained functional connectivity during depolarization, as depolarization block was reduced following fasting. Taken together, inhibitory synaptic transmission from LH GABA inputs onto tVTA/RMTg GABAergic neurons decreases following fasting, however ability to functionally inhibit tVTA/RMTg GABAergic neurons is preserved, allowing for possible disinhibition of dopamine neurons and subsequent foraging.Key PointsWhile dopamine neuronal activity changes with motivational state, it is unknown if fasting influences tVTA/RMTg GABAergic neurons, a major inhibitory input to VTA dopamine neurons.In unfasted mice, there were sex differences in inhibitory synaptic transmission onto tVTA/RMTg GABAergic neurons.Activation of LH GABAergic neurons decreases firing of tVTA/RMTg GABAergic neurons through a monosynaptic input.An acute fast decreased the excitability of tVTA/RMTg GABAergic neurons.An acute fast decreases inhibitory synaptic transmission of the LH GABA input to tVTA/RMTg GABAergic neurons in both male and female mice.

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Neocortex saves energy by reducing coding precision during food scarcity

Cited by 64 publications

References 93 publications

Rational inattention in mice

Rational inattention in mice

Activation of LH GABAergic inputs counteracts fasting‐induced changes in tVTA/RMTG neurons

Activation of LH GABAergic inputs counteracts fasting-induced changes in tVTA/RMTG neurons

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