What can we learn from inactivation studies? Lessons from auditory cortex

Slonina, Zuzanna A.; Poole, Katarina C.; Bizley, Jennifer K.

doi:10.1016/j.tins.2021.10.005

Cited by 20 publications

(29 citation statements)

References 110 publications

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“…The behavioral necessity of a brain area is typically assessed using loss-of-function perturbations. Across sensory modalities, such experiments suggest that primary sensory cortices are essential for some tasks but not others ( Lashley, 1931a , b ; Schneider, 1969 ; Hutson and Masterton, 1986 ; Newsome and Paré, 1988 ; Prusky and Douglas, 2004 ; Glickfeld et al, 2013 ; Shih et al, 2013 ; Poort et al, 2015 ; Goard et al, 2016 ; Resulaj et al, 2018 ; Stüttgen and Schwarz, 2018 ; Slonina et al, 2022 ). Typical loss-of-function experiments inactivate spatially extensive tissue volumes and rarely allow for behavioral recovery, complicating interpretation and leaving open the question of whether small cortical volumes act as permanent perceptual bottlenecks.…”

Section: Introductionmentioning

confidence: 99%

Columnar Lesions in Barrel Cortex Persistently Degrade Object Location Discrimination Performance

Ryan

Laughton²,

Sun-Yan³

et al. 2022

eNeuro

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Primary sensory cortices display functional topography, suggesting that even small cortical volumes may underpin perception of specific stimuli. Traditional loss-of-function approaches have a relatively large radius of effect (>1 mm), and few studies track recovery following loss-of-function perturbations. Consequently, the behavioral necessity of smaller cortical volumes remains unclear. In the mouse primary vibrissal somatosensory cortex (vS1), “barrels” with a radius of ∼150 μm receive input predominantly from a single whisker, partitioning vS1 into a topographic map of well defined columns. Here, we train animals implanted with a cranial window over vS1 to perform single-whisker perceptual tasks. We then use high-power laser exposure centered on the barrel representing the spared whisker to produce lesions with a typical volume of one to two barrels. These columnar-scale lesions impair performance in an object location discrimination task for multiple days without disrupting vibrissal kinematics. Animals with degraded location discrimination performance can immediately perform a whisker touch detection task with high accuracy. Animals trained de novo on both simple and complex whisker touch detection tasks showed no permanent behavioral deficits following columnar-scale lesions. Thus, columnar-scale lesions permanently degrade performance in object location discrimination tasks.

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Section: Introductionmentioning

confidence: 99%

Columnar Lesions in Barrel Cortex Persistently Degrade Object Location Discrimination Performance

Ryan

Laughton²,

Sun-Yan³

et al. 2022

eNeuro

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“…Object location discrimination requires cortex, whereas detection does not. In the auditory cortex, many discrimination behaviors require cortex (Lomber and Malhotra, 2008; Slonina et al, 2022). At the same time, simple auditory features such as frequency can be discriminated even without cortex (Ohl et al, 1999).…”

Section: Discussionmentioning

confidence: 99%

“…The behavioral necessity of a brain area is typically assessed by performing loss-of-function perturbations. Across sensory modalities, such experiments suggest that primary sensory cortices are essential for some tasks but not others (Lashley, 1931a, b; Schneider, 1969; Hutson and Masterton, 1986; Newsome and Pare, 1988; Prusky and Douglas, 2004; Glickfeld et al, 2013; Shih et al, 2013; Poort et al, 2015; Goard et al, 2016; Resulaj et al, 2018; Stuttgen and Schwarz, 2018; Slonina et al, 2022). Traditional loss-of-function perturbations, however, have poor spatial resolution: both transient inactivation (O’Connor et al, 2010; Poort et al, 2015; Goard et al, 2016; Li et al, 2019) and permanent lesions (Lashley, 1931a; Hutson and Masterton, 1986; Resulaj et al, 2018) usually have a radius of effect exceeding 1 mm, thereby impacting hundreds of thousands of neurons.…”

Section: Introductionmentioning

confidence: 99%

Columnar scale lesions in barrel cortex degrade tactile discrimination but not detection

Ryan

Laughton

Sun-Yan

et al. 2022

Preprint

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Primary sensory cortices typically display functional topography, suggesting that even small cortical volumes may underpin perception of specific stimuli. Because traditional loss-of-function approaches have a relatively large radius of effect (>1 mm), the behavioral necessity of smaller cortical volumes remains unclear. In the mouse primary vibrissal somatosensory cortex (vS1), 'barrels' with a radius of ~150 μm receive input predominantly from a single whisker, partitioning vS1 into a topographic map of well- defined columns. Here, we train animals implanted with a cranial window over vS1 to perform single-whisker perceptual tasks. We then use high-power laser exposure centered on the barrel representing the spared whisker to produce lesions with an average volume of ~2 barrels. These columnar scale lesions impair performance on object location discrimination tasks without disrupting vibrissal kinematics. Animals with degraded discrimination performance can immediately perform a detection task with high accuracy. Animals trained de novo on both simple and complex detection tasks showed no behavioral deficits following columnar scale lesions. Thus, vS1 barrels are necessary for performing object location discrimination but not simple or complex object detection

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“…Extensive research has shown how sound localization cues are extracted in the midbrain (Tollin and Yin, 2002;Yin and Chan, 1990) and transmitted across the brain to areas, including auditory cortex (Keating et al, 2015;Stecker et al, 2005), parietal and prefrontal cortex (van der Heijden et al, 2019). While midbrain neurons show tuning to specific localization cues, auditory cortex contains cue-invariant representations of sound location (Wood et al, 2019) and is essential for sound localization in primates and carnivores (Slonina et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

Sound Localization of World and Head-Centered Space in Ferrets

Town

Bizley

2022

J. Neurosci.

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The location of sounds can be described in multiple coordinate systems that are defined relative to ourselves, or the world around us. Evidence from neural recordings in animals point towards the existence of both head-centered and world-centered representations of sound location in the brain; however, it is unclear whether such neural representations have perceptual correlates in the sound localization abilities of non-human listeners. Here, we establish novel behavioral tests to determine the coordinate systems in which ferrets can localize sounds. We found that ferrets could learn to discriminate between sound locations that were fixed in either world-centered or head-centered space, across wide variations in sound location in the alternative coordinate system. Using probe sounds to assess broader generalization of spatial hearing, we demonstrated that in both head and world-centered tasks, animals used continuous maps of auditory space to guide behavior. Single trial responses of individual animals were sufficiently informative that we could then model sound localization using speaker position in specific coordinate systems and accurately predict ferrets' actions in held-out data. Our results indicate that an animal model in which neurons are known to be tuned to sound location in egocentric and allocentric reference frames can also localize sounds in multiple head and world-centered spaces. Significance StatementHumans can describe the location of sounds either relative to themselves, or in the world, independent of their momentary position. These different spaces are also represented in the activity of neurons in animals, but it's not clear whether non-human listeners also perceive both head and world-centered sound location. Here, we designed behavioral tasks in which ferrets discriminated between sounds using their position in the world, or relative to the head. Subjects learnt to solve both problems and generalized sound location in each space when presented with infrequent probe sounds. These findings reveal a perceptual correlate of neural sensitivity previously observed in the ferret brain and establish that, like humans, ferrets can access an auditory map of their local environment.

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What can we learn from inactivation studies? Lessons from auditory cortex

Cited by 20 publications

References 110 publications

Columnar Lesions in Barrel Cortex Persistently Degrade Object Location Discrimination Performance

Columnar Lesions in Barrel Cortex Persistently Degrade Object Location Discrimination Performance

Columnar scale lesions in barrel cortex degrade tactile discrimination but not detection

Sound Localization of World and Head-Centered Space in Ferrets

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