Auditory cortex shapes sound responses in the inferior colliculus

Blackwell, Jennifer M.; Lesicko, Alexandria M.H.; Rao, Winnie; Biasi, Mariella De; Geffen, Maria N.

doi:10.1101/584334

Cited by 4 publications

(8 citation statements)

References 84 publications

(84 reference statements)

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“…Note that, in this study, behavioral data were collected separately from physiological recordings, and recordings were taken from anesthetized animals. No doubt, there are well documented effects of changes in an animal’s attention in neural responses in IC [19] which are probably mediated by corticofugal backprojections [20], but while such rapid, dynamic effects can modulate midbrain tuning, they do not need to be engaged to reveal baseline neural tuning properties which do place constraints on psychoacoustic performance. If that was not the case, the clear parallels between neural and behavioral d’ observed in our study would be very difficult to explain.…”

Section: Discussionmentioning

confidence: 99%

Interaural Time Difference Tuning in the Rat Inferior Colliculus is Predictive of Behavioral Sensitivity

Rajendran

Mishra

et al. 2021

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Recent studies have shown that rats are a useful model for binaural cochlear implant (CI) research, with behavioral sensitivity to interaural time differences (ITDs) of CI stimuli which are better than those of human patients. Here, we characterize ITD tuning in the rat inferior colliculus (IC) and explore whether quality of tuning can predict behavioral performance. We recorded IC responses to stimuli of varying pulse rates and envelope types and quantified both mutual information (MI) and neural d' as measures of ITD sensitivity. Neural d' values paralleled behavioral ones, declining with increasing click rates or when envelopes changed from rectangular to Hanning windows. While MI values increased with experience, neural d' did not. However, neural d' values correlated much better with behavioral performance than MI. Thus, neural d' appears to be a particularly well suited to predicting how stimulus parameters will impact behavioral performance.

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Section: Discussionmentioning

confidence: 99%

Interaural Time Difference Tuning in the Rat Inferior Colliculus is Predictive of Behavioral Sensitivity

Rajendran

Mishra

et al. 2021

Preprint

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“…Best frequency was defined as the frequency with the highest mean response. Sparseness ( S , Equation 2 29,30 ) was used to estimate the sharpness of response functions, with 1 being very sharply tuned and 0 being an equal response to each tone frequency: where r i is the mean response to the frequency i and N is the total number of frequencies tested.…”

Section: Methodsmentioning

confidence: 99%

Neuronal activity in sensory cortex predicts the specificity of learning

Wood

Angeloni

Oxman

et al. 2020

Preprint

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Learning to avoid dangerous signals while preserving normal behavioral responses to safe stimuli is essential for everyday behavior and survival. Like other forms of learning, fear learning has a high level of inter-subject variability. Following an identical fear conditioning protocol, different subjects exhibit a range of fear specificity. Under high specificity, subjects specialize fear to only the paired (dangerous) stimulus, whereas under low specificity, subjects generalize fear to other (safe) sensory stimuli. Pathological fear generalization underlies emotional disorders, such as post-traumatic stress disorder. Despite decades of work, the neuronal basis that determines fear specificity level remains unknown. We identified the neuronal code that underlies variability in fear specificity. We performed longitudinal imaging of activity of neuronal ensembles in the auditory cortex of mice prior to and after the mice were subjected to differential fear conditioning. The neuronal code in the auditory cortex prior to learning predicted the level of specificity following fear learning across subjects. After fear learning, population neuronal responses were reorganized: the responses to the safe stimulus decreased, whereas the responses to the dangerous stimulus remained the same, rather than decreasing as in pseudo-conditioned subjects. The magnitude of these changes, however, did not correlate with learning specificity, suggesting that they did not reflect the fear memory. Together, our results identify a new, temporally restricted, function for cortical activity in associative learning. These results reconcile seemingly conflicting previous findings and provide for a neuronal code for determining individual patterns in learning. Results Experimental setupWhereas AC is involved in auditory fear conditioning, its role in the specificity of fear learning remains controversial. To establish the relationship between sound-evoked activity in the primary auditory cortex and differential fear conditioning (DFC), we recorded simultaneous neural activity from hundreds of neurons. We tracked the same neurons before and after DFC, using two-photon imaging of a virally expressed fluorescent calcium probe (GCaMP6 (Chen et al., 2013), Fig. 1). Longitudinal imaging of neuronal activity in large ensembles of neurons in AC before and after conditioning allowed us to compare the representation of the CS stimuli before and after learning ( Fig. 2A).We conditioned mice by exposure to a sequence of 10 repeats of two tones, one of which coterminated with a foot-shock (CS+, 15 kHz), and one which did not (CS-, 11.4kHz). Pseudo-conditioned mice were presented with the same stimuli (CS, 11.4 kHz and 15 kHz), but the foot-shock occurred during periods of silence between the stimuli (Fig. 2B). We measured recall of the fear memory by presenting the same stimuli to the mouse in a different context and measuring the % of time the mouse froze (Fig. 2C). Learning specificity was defined as a difference between freezing to CS+ and CS-during me...

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“…In a recent experiment in mice using a combination of cortico-anterograde and collicular retrograde viral transfection, it was possible to achieve viral specific transfection of only cortico-collicular neurons ( Blackwell et al, 2020 ). This combination of techniques ensures that only neurons expressing Cre recombinase in the auditory cortex would express ChannelRhodopsine2 (ChR2) or a hyperpolarizing opsin (ArchT) in the auditory cortex.…”

Section: Effects Of the Corticofugal Descending Projectionsmentioning

confidence: 99%

“…This combination of techniques ensures that only neurons expressing Cre recombinase in the auditory cortex would express ChannelRhodopsine2 (ChR2) or a hyperpolarizing opsin (ArchT) in the auditory cortex. Opsins were expressed in AC-IC projecting neurons, and shining light over AC would directly activate, or suppress, only the cortico-collicular feedback projections ( Blackwell et al, 2020 ). ChR2 activation of AC-IC neurons resulted in increasing spontaneous activity in IC neurons with decrease driven activity to pure tones and clicks, but with particularly small effects on magnitude.…”

Section: Effects Of the Corticofugal Descending Projectionsmentioning

confidence: 99%

When and How Does the Auditory Cortex Influence Subcortical Auditory Structures? New Insights About the Roles of Descending Cortical Projections

et al. 2021

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For decades, the corticofugal descending projections have been anatomically well described but their functional role remains a puzzling question. In this review, we will first describe the contributions of neuronal networks in representing communication sounds in various types of degraded acoustic conditions from the cochlear nucleus to the primary and secondary auditory cortex. In such situations, the discrimination abilities of collicular and thalamic neurons are clearly better than those of cortical neurons although the latter remain very little affected by degraded acoustic conditions. Second, we will report the functional effects resulting from activating or inactivating corticofugal projections on functional properties of subcortical neurons. In general, modest effects have been observed in anesthetized and in awake, passively listening, animals. In contrast, in behavioral tasks including challenging conditions, behavioral performance was severely reduced by removing or transiently silencing the corticofugal descending projections. This suggests that the discriminative abilities of subcortical neurons may be sufficient in many acoustic situations. It is only in particularly challenging situations, either due to the task difficulties and/or to the degraded acoustic conditions that the corticofugal descending connections bring additional abilities. Here, we propose that it is both the top-down influences from the prefrontal cortex, and those from the neuromodulatory systems, which allow the cortical descending projections to impact behavioral performance in reshaping the functional circuitry of subcortical structures. We aim at proposing potential scenarios to explain how, and under which circumstances, these projections impact on subcortical processing and on behavioral responses.

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Auditory cortex shapes sound responses in the inferior colliculus

Cited by 4 publications

References 84 publications

Interaural Time Difference Tuning in the Rat Inferior Colliculus is Predictive of Behavioral Sensitivity

Interaural Time Difference Tuning in the Rat Inferior Colliculus is Predictive of Behavioral Sensitivity

Neuronal activity in sensory cortex predicts the specificity of learning

When and How Does the Auditory Cortex Influence Subcortical Auditory Structures? New Insights About the Roles of Descending Cortical Projections

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