Descending and tonotopic projection patterns from the auditory cortex to the inferior colliculus

Straka, Malgorzata; Hughes, Ruth M.; Lee, P.; Lim, Hubert H.

doi:10.1016/j.neuroscience.2015.05.032

Cited by 16 publications

(16 citation statements)

References 64 publications

(119 reference statements)

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“…For this study, experiments were performed on young female Hartley guinea pigs (4-8 weeks, 350-580 g, Elm Hill Breeding Labs, Chelmsford, MA) in accordance with policies of the University of Minnesota Institutional Animal Care and Use Committee. The animal surgical procedures are detailed in previous work (Markovitz et al, 2013;Offutt et al, 2014;Straka et al, 2015). REAGENT activity in the guinea pig auditory cortex (Lim and Anderson, 2007;Middlebrooks, 2008).…”

Section: Star+methodsmentioning

confidence: 99%

“…The input layer of A1 is layer III/IV in guinea pigs (Huang and Winer, 2000;Smith and Populin, 2001), which was identified by performing current source density (CSD) analysis as described in a previous study from our lab (Straka et al, 2015). The one-dimensional CSD approximation provides a consistent representation for the current sinks and sources associated with columnar synaptic…”

Section: Acoustic-driven Responsesmentioning

confidence: 99%

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Ultrasound Produces Extensive Brain Activation via a Cochlear Pathway

Guo

Hamilton

Offutt

et al. 2018

Neuron

230

220

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Ultrasound (US) can noninvasively activate intact brain circuits, making it a promising neuromodulation technique. However, little is known about the underlying mechanism. Here, we apply transcranial US and perform brain mapping studies in guinea pigs using extracellular electrophysiology. We find that US elicits extensive activation across cortical and subcortical brain regions. However, transection of the auditory nerves or removal of cochlear fluids eliminates the US-induced activity, revealing an indirect auditory mechanism for US neural activation. Our findings indicate that US activates the ascending auditory system through a cochlear pathway, which can activate other non-auditory regions through cross-modal projections. This cochlear pathway mechanism challenges the idea that US can directly activate neurons in the intact brain, suggesting that future US stimulation studies will need to control for this effect to reach reliable conclusions.

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Section: Star+methodsmentioning

confidence: 99%

Section: Acoustic-driven Responsesmentioning

confidence: 99%

Ultrasound Produces Extensive Brain Activation via a Cochlear Pathway

Guo

Hamilton

Offutt

et al. 2018

Neuron

230

220

View full text Add to dashboard Cite

show abstract

“…Whereas optogenetic manipulation allows for temporally precise control and cell-type specificity, the technique lacks the spatial specificity of electrical stimulation. Since both AC and cortico-collicular projections are tonotopically organized (Lim and Anderson, 2007;Markovitz et al, 2013;Barnstedt et al, 2015;Straka et al, 2015), spatially specific stimulation can more accurately mimic frequency-specific responses by activating specific regions in the tonotopic map. Previous studies found that electrical stimulation of AC caused best frequencies in IC to shift towards the best frequencies of the stimulated site in AC Suga, 1998, 2000;Yan and Suga, 1998;Ma and Suga, 2001a;Yan et al, 2005;Zhou and Jen, 2007).…”

Section: Discussionmentioning

confidence: 99%

Auditory cortex shapes sound responses in the inferior colliculus

Blackwell

Lesicko

Rao

et al. 2019

Preprint

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The extensive feedback from the auditory cortex (AC) to the inferior colliculus (IC) supports critical aspects of auditory learning, but has not been extensively characterized. Furthermore, it remains unknown whether and how intra-cortical processing of auditory information propagates to earlier stages in the auditory pathway. Previous studies demonstrated that responses of neurons in IC are altered by focal electrical stimulation and pharmacological inactivation of auditory cortex, but these methods lack the ability to selectively manipulate the activity of projection neurons. Combining viral technology with electrophysiological recordings, we measured the effects of selective optogenetic activation or suppression of cortico-collicular feedback projections on IC responses to sounds. Activation of cortico-collicular feedback generally increased spontaneous activity and decreased stimulus selectivity in IC, whereas suppression of the feedback did not affect collicular activity. To further understand how microcircuits in the auditory cortex may control collicular activity, we tested the effects of optogenetically modulating different cortical neuronal subtypes, specifically parvalbumin-positive (PV) and somatostatin-positive (SOM) inhibitory interneurons. We found that, despite strong effects on sound-evoked responses across the layers of AC, activating either type of interneuron did not affect IC sound-evoked activity. However, suppression of SOMs, but not PVs, weakly increased spontaneous activity in IC. These findings suggest that shaping of sound responses mediated by cortical inhibition does not affect sound processing in IC. Combined, our results identify that activation of excitatory projections, but not inhibitory-driven increases in cortical activity, affects collicular sound responses. Significance StatementDescending projections from the auditory cortex to the auditory midbrain, the inferior colliculus, have been shown to play a critical role in auditory learning and behavior. However, little is known about the details of how this direct feedback shapes neuronal responses to sounds in the inferior colliculus. We found that direct activation of cortico-collicular feedback increased spontaneous and modulated sound-evoked activity in the inferior colliculus. Interestingly, modulation of inhibitory interneuron activity, thereby increasing or decreasing excitatory neuronal activity in the auditory cortex, did not affect sound responses in the inferior colliculus. This work offers evidence that auditory cortex shapes sound responses in the inferior colliculus via direct feedback independently of the activity of cortical inhibitory interneurons.

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“…Animal Surgical Preparations: The animal surgical procedures are detailed in previous work (Markovitz et al, 2013;Offutt et al, 2014;Straka et al, 2015). Experiments were performed on thirty young Hartley guinea pigs (350-580 g; Elm Hill Breeding Labs, Chelmsford, MA, USA) in accordance with policies of the University of Minnesota Institutional Animal Care and Use Committee.…”

Section: Methodsmentioning

confidence: 99%

“…For guiding placement of the electrode array into the somatosensory cortex, electrical stimulation of the foot (biphasic, cathodic-leading pulse, 205 µs/phase, levels of 2.82 mA) with the stimulation ground placed in the foot was used. The input layer of A1 is layer III/IV in guinea pigs (Huang and Winer, 2000;Smith and Populin, 2001), which was identified by performing current source density (CSD) analysis as described in one previous study from our lab (Straka et al, 2015). The one-dimensional CSD approximation provides a consistent representation for the current sinks and sources associated with columnar synaptic activity in the guinea pig auditory cortex (Lim and Anderson, 2007;Middlebrooks, 2008).…”

Section: Methodsmentioning

confidence: 99%

Ultrasound Produces Extensive Brain Activation via a Cochlear Pathway

Guo

Hamilton

Offutt

et al. 2017

Preprint

View full text Add to dashboard Cite

SummaryUltrasound (US) can noninvasively activate intact brain circuits, making it a promising neuromodulation technique. However, little is known about the underlying mechanism. Here, we apply transcranial US and perform brain mapping studies in guinea pigs using extracellular electrophysiology. We find that US elicits extensive activation across cortical and subcortical brain regions. However, transection of the auditory nerves or removal of cochlear fluids eliminates the US-induced activity, revealing an indirect auditory mechanism for US neural activation. US likely vibrates the cerebrospinal fluid in the brain, which is continuous with the fluid in the cochlea via cochlear aqueducts; thus, US can activate the ascending auditory pathways and other non-auditory regions through cross-modal projections. This finding of a cochlear fluidinduced vibration mechanism challenges the idea that US can directly activate neurons in the intact brain, suggesting that future US stimulation studies will need to control for this effect to reach reliable conclusions.peer-reviewed)

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Descending and tonotopic projection patterns from the auditory cortex to the inferior colliculus

Cited by 16 publications

References 64 publications

Ultrasound Produces Extensive Brain Activation via a Cochlear Pathway

Ultrasound Produces Extensive Brain Activation via a Cochlear Pathway

Auditory cortex shapes sound responses in the inferior colliculus

Ultrasound Produces Extensive Brain Activation via a Cochlear Pathway

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