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1622 • The Journal of Neuroscience, February 24, 2021 • 41(8):1622–1624

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An Auditory Phantom Percept That Does Not Impair External

Kameron K. Clayton1,2 and Elouise A. Koops2,3 1Speech and Bioscience and Technology Program, Division of Medical Sciences, Harvard Medical School, Boston, Massachusetts 02114, 2Eaton-Peabody Laboratories, Massachusetts Eye and Infirmary, Boston, Massachusetts 02114, and 3Department of Otolaryngology – Head and Neck Surgery, Harvard Medical School, Boston, Massachusetts 02114 Review of Zeng et al.

To accurately represent the world, the Astumblingblockinunderstanding have attempted to use the acoustic startle must distinguish between inter- the neural basis of is a methodo- reflex to diagnose the presence of tinni- nally generated activity and activity logical mismatch between and ani- tus in animals. Indeed, gap-based pre- evoked by external stimuli. When inter- mal studies. While it is straightforward for pulse inhibition of the acoustic startle nal brain dynamics mimic - to report their subjective experi- reflex is impaired after peripheral dam- evoked activity patterns, phantom per- ence, techniques for recording from the age to the auditory system across multi- ception may occur (Kenet et al., 2003). human brain lack sufficient resolution to ple animal models (Longenecker et al., One common form of phantom percep- identify the neural circuits responsible for 2018). However, evidence of impaired tion is tinnitus, the perception of sound tinnitus. Conversely, in animals where it is gap detection in humans is lacking in the absence of an external acoustic possible to record neural activity with cel- (Boyen et al., 2015). source. Generally, tinnitus emerges as a lular resolution and cell-type specificity, A recent study by Zeng et al. (2020) sequela of damage to the auditory pe- it is difficult to devise behavioral tasks systematically tested whether tinnitus riphery. In response to decreased periph- that unambiguously indicate animals are interfered with gap detection and other eral input, neurons throughout the experiencing tinnitus-like percepts. One aspects of auditory perception across central auditory pathway increase their potentially powerful way to bridge the many behavioral tasks and stimulus pa- spontaneous firing rates and sensory gap between human and animal studies rameters in human listeners. To optimize response gain (Eggermont and Roberts, is to test whether tinnitus percepts inter- interference between tinnitus and external 2004). However, tinnitus develops in fere with auditory perception, because stimuli, the authors first had to quantify ’ only approximately half of individuals perceptual abilities are measurable in what each individual s tinnitus sounded with , and, conversely, tin- both humans and animals. Because tinni- like. To identify individual tinnitus per- nitus can emerge after only subtle dam- tus percepts can be modulated by the cepts, subjects matched an external tone age to the (Schaette and presence of external sound (Feldmann, to their tinnitus in both frequency and McAlpine, 2011). Thus, while hyperac- 1971), it is plausible that tinnitus per- level. Consistent with previous work, tivity and hyperexcitability throughout cepts might also interfere with the proc- tinnitus percepts were most commonly essing of external . matched to high-frequency (;4kHz), the central auditory pathway are associ- ; ated with tinnitus generation, the pre- One important aspect of sound proc- low-level tones ( 10 dB above hearing cise neurobiological basis of tinnitus essing is gap detection. Brief silent gaps thresholds; Moore, 2012). remains unknown. in sounds are critical cues for auditory To address whether tinnitus fills in scene analysis and speech perception. gaps in sound for human listeners, Zeng et Gaps in ongoing sound can also attenu- al. (2020) used an adaptive procedure to Received Sep. 28, 2020; revised Dec. 22, 2020; accepted Dec. 23, 2020. ate the acoustic startle reflex induced by estimate gap detection thresholds across a We thank Meenakshi Asokan, Matthew McGill, and Dr. Ross intense sounds. Tinnitus might fill in range of sound frequencies. Gap detection Williamson for feedback on an earlier version of this article. these silent gaps, thus rendering them thresholds in tinnitus subjects were com- Correspondence should be addressed to Kameron K. Clayton at [email protected]. inaudible. If this occurs, tinnitus might parable to those in control subjects, even https://doi.org/10.1523/JNEUROSCI.2528-20.2020 blunt gap-induced attenuation of the for tones matched to individual tinnitus Copyright © 2021 the authors startle reflex. Therefore, previous studies frequencies and levels. Not only does the Clayton and Koops · Tinnitus Does Not Impair Auditory Perception J. Neurosci., February 24, 2021 • 41(8):1622–1624 • 1623 absence of impairment in tinnitus subjects resource, any attention devoted to tinni- because of redundancy with the ventral cast doubt on behavioral approaches based tus might limit attentional resources that nucleus (Masterton and Granger, 1988). on gap detection in animal models, it also could be deployed to multiple competing This example illustrates a general princi- suggests that the neural generator of tinni- external stimuli. Consistent with this ple: wherever in the auditory pathway tus is independent from pathways for the prediction, previous studies in humans the neural activity underlying tinnitus perception of external sounds. and animals have suggested that tinnitus emerges, there are other parallel and Given that gap detection was not subjects perform worse than control redundant loci which could subserve the impaired, the authors asked whether subjects in auditory and nonauditory normal perception of external stimuli de- other facets of auditory perception would selective attention tasks (Brozoski et al., spite ongoing neural activity related to reveal interactions between internal tin- 2019). Further, human neuroimaging the phantom percept. nitus percepts and the perception of studies suggest that nonauditory areas In summary, Zeng et al. (2020) present external stimuli. Even near their individ- involved in attentional control, such as compelling behavioral evidence that audi- ual tinnitus frequencies, tinnitus patients the anterior cingulate cortex, precuneus, tory perception is not impaired by tinni- were as adept as control subjects at dis- and hippocampus, show heightened ac- tus. These results draw into question criminating tiny differences in sound fre- tivity in tinnitus subjects (Roberts et al., widely used animal behavioral models and quency. Further, across multiple sound 2013). Future studies that parametrically constrain theoretical accounts of the neu- levels, tinnitus subjects were equal or bet- vary attentional demands should clarify robiological basis of tinnitus. Converging ter than control subjects in sound inten- exactly how tinnitus captures attention. evidence suggests that tinnitus may be as sity discrimination. More perceptually Importantly, the finding that audi- much a disorder of attention as it is one demanding tasks, including tone in noise tory perception is not impaired in tinni- of damage to the auditory periphery. detection, temporal modulation detec- tus subjects also constrains theories Understanding how attention interacts tion, and speech in noise recognition, of the neural circuits underlying tinni- with tinnitus perception will be crucial to also failed to reveal a deficit in tinnitus tus. Redundant distributed neural codes developing effective therapies for this subjects. The lack of differences across all for external sound coupled with sparse pervasive auditory disorder. tested tasks and stimuli is striking, lead- local codes for internally generated tin- ing the authors to suggest that tinnitus nitus percepts could explain the percep- References and external sound have an asymmetrical tual asymmetry that Zeng et al. (2020) Boyen K, Bas¸kent D, van Dijk P (2015) The gap relationship: while in most cases tinnitus observed. External sounds recruit par- detection test: can it be used to diagnose tinni- can be masked by external sounds, tinni- tially redundant ascending pathways ter- tus?EarHear36:e138–e145. tus does not seem to interfere with per- minating in multiple areas across both Brozoski T, Wisner K, Randall M, Caspary D ception of external sound. hemispheres of the (Levy (2019) Chronic sound-induced tinnitus and To explain the asymmetry in how ex- et al., 2019). Yet, studies in other sensory auditory attention in animals. Neuroscience 407:200–212. ternally and internally generated percepts systems suggest that animals can attend Eggermont JJ, Roberts LE (2004) The neuro- interact, Zeng et al. (2020) propose a sim- to and behaviorally report artificial stim- science of tinnitus. Trends Neurosci 27:676– ple attention normalization model with ulation of single neurons or small ensem- 682. two channels, one representing the “top- bles (Houweling and Brecht, 2008; Gill et Feldmann H (1971) Homolateral and contralateral down” tinnitus signal and the other repre- al., 2020). The percept of tinnitus might masking of tinnitus by noise-bands and by senting a physical stimulus, inspired by similarly emerge from hyperactivity or pure tones. 10:138–144. models of visual attention (Reynolds and hypersynchrony in small ensembles of Gill JV, Lerman GM, Zhao H, Stetler BJ, Rinberg D, Shoham S (2020) Precise holographic Heeger, 2009). In the model, the total per- auditory neurons in the absence of exter- manipulation of olfactory circuits reveals cod- cept of the observer is the weighted sum of nal sound. Consistent with the proposal ing features determining perceptual detection. attention to tinnitus and attention to the of Zeng et al. (2020), sparse codes for Neuron 108:382–393.e5. stimulus. In the absence of external stim- phantom percepts likely require atten- Houweling AR, Brecht M (2008) Behavioural uli, the total percept is dominated by tinni- tion or top-down feedback to rise to the report of single neuron stimulation in somato- – tus, as all attention is allocated to the level of conscious (Van Vugt . Nature 451:65 68. phantom percept. The primary insight of et al., 2018). At the same time, these KenetT,BibitchkovD,TsodyksM,GrinvaldA, Arieli A (2003) Spontaneously emerging corti- the model is that while keeping attention sparse local codes for phantom percepts cal representations of visual attributes. Nature to tinnitus fixed, increasing attention to are unlikely to interfere with external 425:954–956. the external stimulus can attenuate the sound perception arising through multi- Levy RB, Marquarding T, Reid AP, Pun CM, perceived tinnitus loudness by up to a fac- ple parallel pathways. Renier N, Oviedo HV (2019) Circuit asym- tor of five. The model suggests that engag- As a concrete example, consider the metries underlie functional lateralization in ing in near-threshold perceptual tasks first station of the central auditory path- the mouse . Nat Commun could direct attention away from the tinni- way, the , which consists 10:2783. Longenecker RJ, Kristaponyte I, Nelson GL, tus percept, possibly accounting for the of a dorsal and a ventral subdivision, Young JW, Galazyuk AV (2018) Addressing lack of differences between tinnitus sub- both of which receive input from the au- variability in the acoustic startle reflex for accu- jects and controls across many measures ditory nerve. Increased spontaneous fir- rate gap detection assessment. Hear Res of auditory perception. ing and synchrony in dorsal cochlear 363:119–135. While subjects may be able to steer nucleus neurons after damage to the au- Masterton RB, Granger EM (1988) Role of the their attention away from tinnitus during ditory periphery is central to theories of tin- acoustic striae in hearing: contribution of dor- sal and intermediate striae to detection of basic perceptual tasks, the model proposed nitus generation (Shore and Wu, 2019). noises and tones. J Neurophysiol 60:1841– by Zeng et al. (2020) predicts that tinnitus Yet, lesions to the dorsal cochlear nu- 1860. would incur a cost in more attentionally cleus fail to produce deficits across numer- Moore B (2012) The psychophysics of tinnitus. In: demanding tasks. If attention is a finite ous auditory perceptual tasks, presumably Tinnitus (Eggermont JJ, Zeng F-G, Fay R, 1624 • J. Neurosci., February 24, 2021 • 41(8):1622–1624 Clayton and Koops · Tinnitus Does Not Impair Auditory Perception

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