Auditory Midbrain Encodes Behavioral Responses Independently of Cortical Input

Core Concepts

The inferior colliculus, a midbrain auditory structure, can encode information about an animal's behavioral responses to sound stimuli independently of input from the auditory cortex.

Abstract

The study investigated the activity of neurons in the inferior colliculus (IC), a midbrain auditory structure, in mice performing a sound detection task. The authors used a transsynaptic labeling approach to specifically target and image corticorecipient neurons in the IC shell, which receive direct input from the auditory cortex. Key findings: The majority of corticorecipient IC neurons exhibited distinct activity patterns for hit vs. miss trials, indicating they encoded information beyond just the physical attributes of the sound stimulus. Trial-by-trial behavioral outcomes could be accurately decoded from the population activity of these IC neurons, both in mice with an intact auditory cortex and in mice with bilateral lesions of the auditory cortex. Mice with complete auditory cortex lesions showed similar decoding performance as non-lesioned mice, suggesting the IC can generate rich representations of behavioral variables independently of cortical input. Partial lesions of the auditory cortex led to reduced decoding performance, potentially due to disruptive effects of residual cortical input. These findings demonstrate that the auditory midbrain, specifically the IC, has access to a wealth of non-acoustic information that can support sound detection behavior, even in the absence of input from the auditory cortex. This challenges the classical view of a strict hierarchical flow of information from the sensory periphery to the cortex and highlights the importance of subcortical processing in sensory perception and behavior.

Stats

"The activity of individual corticorecipient IC neurons showed distinct response profiles across neurons and trial outcomes (hit vs miss)." "Close to half (1272 / 2649) of all neurons showed a statistically significant difference in response magnitude between hit and miss trials, while only a small fraction (97 / 2649) exhibited a significant response to the sound." "The average decoding performance for mice with (near-)complete lesions was significantly better than that measured for mice with partial lesions."

Quotes

"Surprisingly, this was also the case in mice in which auditory cortical input to the midbrain had been removed by bilateral cortical lesions." "These findings suggest that subcortical auditory structures have access to a wealth of non-auditory information independently of descending inputs from the auditory cortex." "Consequently, the contextually-enriched representations that are characteristic of sensory cortices can arise from subcortical processing."

Key Insights Distilled From

Midbrain encodes sound detection behavior without auditory cortex

by Lee,T.-Y., W... at www.biorxiv.org 06-07-2023

https://www.biorxiv.org/content/10.1101/2023.06.07.544013v3

Deeper Inquiries

How might the auditory midbrain acquire and integrate non-acoustic information in the absence of cortical input?

In the absence of cortical input, the auditory midbrain can acquire and integrate non-acoustic information through various alternative pathways and mechanisms. One key mechanism is through direct connections with other sensory modalities and brain regions. Subcortical auditory structures, including the midbrain, receive inputs from multiple sensory pathways, such as somatosensory and visual pathways, allowing them to integrate non-auditory information. These inputs can provide contextual information, motor signals, and neuromodulatory inputs that shape the activity of midbrain neurons. Additionally, the midbrain can also rely on intrinsic circuitry and feedback loops within the auditory system to process non-acoustic information. Local circuits within the midbrain can generate complex neural representations based on a combination of sensory inputs and internal states. These circuits can undergo plasticity and adaptation to encode and integrate non-acoustic information effectively. Furthermore, the midbrain may utilize subcortical pathways and structures, such as the thalamus and brainstem nuclei, to receive and process non-auditory information. These pathways can relay information from higher-order brain regions and sensory modalities to the midbrain, allowing for the integration of diverse inputs and the generation of contextually enriched representations. Overall, the auditory midbrain can acquire and integrate non-acoustic information through a combination of direct sensory inputs, intrinsic circuitry, and subcortical pathways, enabling it to generate complex neural representations and support adaptive behavior in the absence of cortical input.

How might the auditory midbrain acquire and integrate non-acoustic information in the absence of cortical input?

Partial auditory cortex lesions could have a more disruptive effect on midbrain representations compared to complete lesions due to several potential mechanisms. One possible mechanism is the presence of residual and aberrant cortical activity in the remaining tissue after partial lesions. This aberrant activity may interfere with normal processing and communication within the auditory cortex and its downstream targets, leading to disrupted neural representations in the midbrain. Additionally, partial lesions may disrupt the balance of excitation and inhibition within the auditory cortex, affecting the overall neural activity patterns and information processing. The presence of partially lesioned areas with altered neural dynamics could lead to inconsistent or conflicting signals being transmitted to the midbrain, impacting the integration of non-acoustic information and the generation of contextually relevant representations. Moreover, the size and location of partial lesions may result in the preservation of specific cortical circuits or functions that are critical for midbrain processing. The disruption of these specific circuits, while leaving others intact, could lead to a more pronounced impact on midbrain representations compared to complete lesions, where all cortical inputs are eliminated uniformly. Overall, partial auditory cortex lesions may have a more disruptive effect on midbrain representations due to the presence of residual aberrant activity, alterations in excitation-inhibition balance, and the preservation or disruption of specific cortical circuits critical for midbrain processing.

What are the broader implications of these findings for our understanding of the role of the auditory cortex in sound perception and behavior?

These findings have significant implications for our understanding of the role of the auditory cortex in sound perception and behavior. The results suggest that the auditory midbrain, particularly the IC, can independently acquire and integrate non-acoustic information to support sound detection behavior in the absence of cortical input. This challenges the traditional view that the auditory cortex is essential for integrating contextual information and shaping neural representations in subcortical auditory structures. The findings also highlight the complexity and redundancy of neural circuits involved in sound perception and behavior. The ability of the midbrain to generate contextually enriched representations and support adaptive behavior without cortical input underscores the robustness and flexibility of the auditory system. It suggests that multiple pathways and mechanisms exist for processing sensory information and generating appropriate behavioral responses. Furthermore, these findings raise questions about the specific contributions of the auditory cortex to sound perception and behavior. While the auditory cortex is known to play a crucial role in processing complex auditory stimuli and integrating sensory information, its necessity for basic sound detection tasks may be more limited than previously thought. This challenges the conventional hierarchy of sensory processing and emphasizes the distributed nature of neural processing in the auditory system. Overall, these findings broaden our understanding of the functional organization of the auditory system and highlight the dynamic and adaptive nature of neural circuits involved in sound perception and behavior.