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Tonotopic organization in the depth of human inferior colliculus.

ABSTRACT: Experiments in animal models indicate that inferior colliculus (IC), the primary auditory midbrain structure, represents sound frequency in a particular spatial organization, a tonotopy, that proceeds from dorsal and superficial to ventral and deeper tissue. Experiments are presented that use high-resolution, sparse-sampling functional magnetic resonance imaging (fMRI) at 3 T to determine if tonotopic gradients can be reliably measured in human IC using high-resolution fMRI. Stimuli were sequences of bandpass-filtered noise with different center frequencies, presented sequentially while fMRI data were collected. Four subjects performed an adaptive frequency-discrimination task throughout the experiment. Results show statistically significant tonotopic gradients within both ICs of all subjects. Frequency gradients as a function of depth were measured using surface-based analysis methods that make virtual penetrations into the IC tissue. This organization was evident over substantial portions of the IC, at locations that are consistent with the expected location of the central nucleus of IC. The results confirm a laminar tonotopy in the human IC at 3 T, but with a heterogeneous, patchy character. The success of these surface-based analysis methods will enable more detailed non-invasive explorations of the functional architecture of other subcortical human auditory structures that have complex, laminar organization.

SUBMITTER: Ress D

PROVIDER: S-EPMC3776955 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The inferior colliculus (IC) is a critical integration center in the auditory pathway. However, because the inputs to the IC have typically been studied by the use of conventional anterograde and retrograde tracers, the neuronal organization and cell-type-specific connections in the IC are poorly understood. Here, we used monosynaptic rabies tracing and in situ hybridization combined with excitatory and inhibitory Cre transgenic mouse lines of both sexes to characterize the brainwide and cell-type-specific inputs to specific neuron types within the lemniscal IC core and nonlemniscal IC shell. We observed that both excitatory and inhibitory neurons of the IC shell predominantly received ascending inputs rather than descending or core inputs. Correlation and clustering analyses revealed two groups of excitatory neurons in the shell: one received inputs from a combination of ascending nuclei, and the other received inputs from a combination of descending nuclei, neuromodulatory nuclei, and the contralateral IC. In contrast, inhibitory neurons in the core received inputs from the same combination of all nuclei. After normalizing the extrinsic inputs, we found that core inhibitory neurons received a higher proportion of inhibitory inputs from the ventral nucleus of the lateral lemniscus than excitatory neurons. Furthermore, the inhibitory neurons preferentially received inhibitory inputs from the contralateral IC shell. Because IC inhibitory neurons innervate the thalamus and contralateral IC, the inhibitory inputs we uncovered here suggest two long-range disinhibitory circuits. In summary, we found: (1) dominant ascending inputs to the shell, (2) two subpopulations of shell excitatory neurons, and (3) two disinhibitory circuits.SIGNIFICANCE STATEMENT Sound undergoes extensive processing in the brainstem. The inferior colliculus (IC) core is classically viewed as the integration center for ascending auditory information, whereas the IC shell integrates descending feedback information. Here, we demonstrate that ascending inputs predominated in the IC shell but appeared to be separated from the descending inputs. The presence of inhibitory projection neurons is a unique feature of the auditory ascending pathways, but the connections of these neurons are poorly understood. Interestingly, we also found that inhibitory neurons in the IC core and shell preferentially received inhibitory inputs from ascending nuclei and contralateral IC, respectively. Therefore, our results suggest a bipartite domain in the IC shell and disinhibitory circuits in the IC.

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Tonotopic organization in the depth of human inferior colliculus.

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