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Cortical modulation of auditory processing in the midbrain.

Bajo VM, King AJ - Front Neural Circuits (2013)

Bottom Line: Focal electrical stimulation and inactivation studies have shown that the auditory cortex can modify almost every aspect of the response properties of IC neurons, including their sensitivity to sound frequency, intensity, and location.Along with other descending pathways in the auditory system, the corticocollicular projection appears to continually modulate the processing of acoustical signals at subcortical levels.In particular, there is growing evidence that these circuits play a critical role in the plasticity of neural processing that underlies the effects of learning and experience on auditory perception by enabling changes in cortical response properties to spread to subcortical nuclei.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Anatomy and Genetics, University of Oxford Oxford, UK.

ABSTRACT
In addition to their ascending pathways that originate at the receptor cells, all sensory systems are characterized by extensive descending projections. Although the size of these connections often outweighs those that carry information in the ascending auditory pathway, we still have a relatively poor understanding of the role they play in sensory processing. In the auditory system one of the main corticofugal projections links layer V pyramidal neurons with the inferior colliculus (IC) in the midbrain. All auditory cortical fields contribute to this projection, with the primary areas providing the largest outputs to the IC. In addition to medium and large pyramidal cells in layer V, a variety of cell types in layer VI make a small contribution to the ipsilateral corticocollicular projection. Cortical neurons innervate the three IC subdivisions bilaterally, although the contralateral projection is relatively small. The dorsal and lateral cortices of the IC are the principal targets of corticocollicular axons, but input to the central nucleus has also been described in some studies and is distinctive in its laminar topographic organization. Focal electrical stimulation and inactivation studies have shown that the auditory cortex can modify almost every aspect of the response properties of IC neurons, including their sensitivity to sound frequency, intensity, and location. Along with other descending pathways in the auditory system, the corticocollicular projection appears to continually modulate the processing of acoustical signals at subcortical levels. In particular, there is growing evidence that these circuits play a critical role in the plasticity of neural processing that underlies the effects of learning and experience on auditory perception by enabling changes in cortical response properties to spread to subcortical nuclei.

No MeSH data available.


Corticofugal modulation of IC response properties. (A) Lateral view of the brain of a mustached bat, one of the species used most in cortical stimulation and inactivation experiments. The auditory cortex has reciprocal ascending and descending connections with the medial geniculate body (MGB) in the thalamus. It also sends a descending projection to the IC, which, in turn, projects to the MGB. (B) Focal electrical stimulation in the cortex results in facilitation of the responses of IC neurons that have tuning properties matched to those of cortical neurons at the site of the stimulating electrode. The tuning of unmatched IC neurons may shift toward that of the stimulated cortical neurons (as illustrated here), resulting in an expanded representation of the stimulus feature. Shifts in tuning away from that of the stimulated cortical neurons have also been described, compressing the midbrain representation. Adapted with permission from Suga (2012).
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Figure 7: Corticofugal modulation of IC response properties. (A) Lateral view of the brain of a mustached bat, one of the species used most in cortical stimulation and inactivation experiments. The auditory cortex has reciprocal ascending and descending connections with the medial geniculate body (MGB) in the thalamus. It also sends a descending projection to the IC, which, in turn, projects to the MGB. (B) Focal electrical stimulation in the cortex results in facilitation of the responses of IC neurons that have tuning properties matched to those of cortical neurons at the site of the stimulating electrode. The tuning of unmatched IC neurons may shift toward that of the stimulated cortical neurons (as illustrated here), resulting in an expanded representation of the stimulus feature. Shifts in tuning away from that of the stimulated cortical neurons have also been described, compressing the midbrain representation. Adapted with permission from Suga (2012).

Mentions: These studies have provided considerable evidence that corticofugal inputs make an important contribution to the response properties of neurons at multiple subcortical levels. In the IC, neuronal sensitivity to sound frequency (Ma and Suga, 2001a; Yan et al., 2005), intensity (Yan and Ehret, 2002), duration (Ma and Suga, 2001b), and location (Zhou and Jen, 2005; Nakamoto et al., 2008) changes after manipulating activity in A1 (Figures 7, 8). Thus, the descending system can shape the way midbrain neurons respond to stimulus attributes, such as sound frequency or intensity, which are initially encoded in the cochlea, as well as those that rely on central processing, like sound source location. This suggests that cortical feedback is likely to influence the representation of multiple sound features in the midbrain, implying widespread effects on auditory perception. Recent research also suggests that the auditory cortex modulates collicular processing of simultaneously presented harmonic complexes, suggesting a possible role for descending projections in segregating different sound sources (Nakamoto et al., 2010).


Cortical modulation of auditory processing in the midbrain.

Bajo VM, King AJ - Front Neural Circuits (2013)

Corticofugal modulation of IC response properties. (A) Lateral view of the brain of a mustached bat, one of the species used most in cortical stimulation and inactivation experiments. The auditory cortex has reciprocal ascending and descending connections with the medial geniculate body (MGB) in the thalamus. It also sends a descending projection to the IC, which, in turn, projects to the MGB. (B) Focal electrical stimulation in the cortex results in facilitation of the responses of IC neurons that have tuning properties matched to those of cortical neurons at the site of the stimulating electrode. The tuning of unmatched IC neurons may shift toward that of the stimulated cortical neurons (as illustrated here), resulting in an expanded representation of the stimulus feature. Shifts in tuning away from that of the stimulated cortical neurons have also been described, compressing the midbrain representation. Adapted with permission from Suga (2012).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3539853&req=5

Figure 7: Corticofugal modulation of IC response properties. (A) Lateral view of the brain of a mustached bat, one of the species used most in cortical stimulation and inactivation experiments. The auditory cortex has reciprocal ascending and descending connections with the medial geniculate body (MGB) in the thalamus. It also sends a descending projection to the IC, which, in turn, projects to the MGB. (B) Focal electrical stimulation in the cortex results in facilitation of the responses of IC neurons that have tuning properties matched to those of cortical neurons at the site of the stimulating electrode. The tuning of unmatched IC neurons may shift toward that of the stimulated cortical neurons (as illustrated here), resulting in an expanded representation of the stimulus feature. Shifts in tuning away from that of the stimulated cortical neurons have also been described, compressing the midbrain representation. Adapted with permission from Suga (2012).
Mentions: These studies have provided considerable evidence that corticofugal inputs make an important contribution to the response properties of neurons at multiple subcortical levels. In the IC, neuronal sensitivity to sound frequency (Ma and Suga, 2001a; Yan et al., 2005), intensity (Yan and Ehret, 2002), duration (Ma and Suga, 2001b), and location (Zhou and Jen, 2005; Nakamoto et al., 2008) changes after manipulating activity in A1 (Figures 7, 8). Thus, the descending system can shape the way midbrain neurons respond to stimulus attributes, such as sound frequency or intensity, which are initially encoded in the cochlea, as well as those that rely on central processing, like sound source location. This suggests that cortical feedback is likely to influence the representation of multiple sound features in the midbrain, implying widespread effects on auditory perception. Recent research also suggests that the auditory cortex modulates collicular processing of simultaneously presented harmonic complexes, suggesting a possible role for descending projections in segregating different sound sources (Nakamoto et al., 2010).

Bottom Line: Focal electrical stimulation and inactivation studies have shown that the auditory cortex can modify almost every aspect of the response properties of IC neurons, including their sensitivity to sound frequency, intensity, and location.Along with other descending pathways in the auditory system, the corticocollicular projection appears to continually modulate the processing of acoustical signals at subcortical levels.In particular, there is growing evidence that these circuits play a critical role in the plasticity of neural processing that underlies the effects of learning and experience on auditory perception by enabling changes in cortical response properties to spread to subcortical nuclei.

View Article: PubMed Central - PubMed

Affiliation: Department of Physiology, Anatomy and Genetics, University of Oxford Oxford, UK.

ABSTRACT
In addition to their ascending pathways that originate at the receptor cells, all sensory systems are characterized by extensive descending projections. Although the size of these connections often outweighs those that carry information in the ascending auditory pathway, we still have a relatively poor understanding of the role they play in sensory processing. In the auditory system one of the main corticofugal projections links layer V pyramidal neurons with the inferior colliculus (IC) in the midbrain. All auditory cortical fields contribute to this projection, with the primary areas providing the largest outputs to the IC. In addition to medium and large pyramidal cells in layer V, a variety of cell types in layer VI make a small contribution to the ipsilateral corticocollicular projection. Cortical neurons innervate the three IC subdivisions bilaterally, although the contralateral projection is relatively small. The dorsal and lateral cortices of the IC are the principal targets of corticocollicular axons, but input to the central nucleus has also been described in some studies and is distinctive in its laminar topographic organization. Focal electrical stimulation and inactivation studies have shown that the auditory cortex can modify almost every aspect of the response properties of IC neurons, including their sensitivity to sound frequency, intensity, and location. Along with other descending pathways in the auditory system, the corticocollicular projection appears to continually modulate the processing of acoustical signals at subcortical levels. In particular, there is growing evidence that these circuits play a critical role in the plasticity of neural processing that underlies the effects of learning and experience on auditory perception by enabling changes in cortical response properties to spread to subcortical nuclei.

No MeSH data available.