A stable sensory map emerges from a dynamic equilibrium of neurons with unstable tuning properties

Abstract

Recent long-term measurements of neuronal activity have revealed that, despite stability in large-scale topographic maps, the tuning properties of individual cortical neurons can undergo substantial reformatting over days. To shed light on this apparent contradiction, we captured the sound response dynamics of auditory cortical neurons using repeated 2-photon calcium imaging in awake mice. We measured sound-evoked responses to a set of pure tone and complex sound stimuli in more than 20,000 auditory cortex neurons over several days. We found that a substantial fraction of neurons dropped in and out of the population response. We modeled these dynamics as a simple discrete-time Markov chain, capturing the continuous changes in responsiveness observed during stable behavioral and environmental conditions. Although only a minority of neurons were driven by the sound stimuli at a given time point, the model predicts that most cells would at least transiently become responsive within 100 days. We observe that, despite single-neuron volatility, the population-level representation of sound frequency was stably maintained, demonstrating the dynamic equilibrium underlying the tonotopic map. Our results show that sensory maps are maintained by shifting subpopulations of neurons “sharing” the job of creating a sensory representation.

Representational drift in barrel cortex is receptive field dependent

“…We next examined the relative stability of subpopulation membership for individual neurons, looking both at what neurons belonging to a given subpopulation became on subsequent sessions ( Figure 5A ) and which subpopulation a neuron belonged to in prior sessions ( Figure 5B ). We quantified stability by calculating the frequency with which neurons changed touch subpopulation 25 ( Figure 5C ). Neurons that were non-touch responsive or unidirectional single whisker on a given session were most likely to have been non-touch responsive on the prior session.…”

Nonlinear sensitivity to acoustic context is a stable feature of neuronal responses to complex sounds in auditory cortex of awake mice

“…Other electrophysiological studies focusing on more basic measures of stimulus selectivity, such as frequency tuning, have suggested that neuronal response properties may be stable for days or weeks in awake animals implanted with electrode arrays (Williams et al, 1999;Witte et al, 1999). More recently, in vivo two-photon calcium imaging has been used to track sound-evoked responses of auditory cortical neurons across many days (Kato et al, 2015;Aschauer et al, 2022;Chambers et al, 2022). Selectivity for simple and complex sounds was reported to be relatively stable across days at the population level but unstable at the single-neuron level (Aschauer et al, 2022;Chambers et al, 2022).…”

“…More recently, in vivo two-photon calcium imaging has been used to track sound-evoked responses of auditory cortical neurons across many days (Kato et al, 2015;Aschauer et al, 2022;Chambers et al, 2022). Selectivity for simple and complex sounds was reported to be relatively stable across days at the population level but unstable at the single-neuron level (Aschauer et al, 2022;Chambers et al, 2022). Much of this instability in single-neuron stimulus selectivity appears to arise from frequently quiescent neurons that might not be detected in electrophysiological studies; more active neurons may maintain more consistent stimulus selectivity.…”

“…Aschauer et al, 2022;Chambers et al, 2022) -and these have used two-photon calcium imaging, which provides an indirect measure of spiking activity with low temporal resolution and therefore can be used only to assess selectivity for different complex sounds, not to map the detailed structure of receptive fields. These imaging studies have reported that selectivity of cortical neurons for complex stimuli fluctuates across days(Chambers et al, 2022), and that stability of cortical representations depends in part on the behavioral significance of the stimuli(Aschauer et al, 2022).…”

“…Aschauer et al, 2022;Chambers et al, 2022) -and these have used two-photon calcium imaging, which provides an indirect measure of spiking activity with low temporal resolution and therefore can be used only to assess selectivity for different complex sounds, not to map the detailed structure of receptive fields. These imaging studies have reported that selectivity of cortical neurons for complex stimuli fluctuates across days(Chambers et al, 2022), and that stability of cortical representations depends in part on the behavioral significance of the stimuli(Aschauer et al, 2022). Meanwhile, previous electrophysiological studies of neuronal responses to complex sounds have found that spectrotemporal receptive fields (analogous to PRFs, not CGFs) are stable over minutes to hours of recording in awake passively listening animals(Elhilali et al, 2007;Grana et al, 2009), but are substantially modified by engagement in behavior (e.g.,Fritz et al, 2005;David et al, 2012).…”