Behavioral/Systems/CognitiveSelective Attention to Visual Stimuli Reduces CochlearSensitivity in ChinchillasPaul H. Delano, Diego Elgueda, Carlos M. Hamame, and Luis RoblesPrograma de Fisiologı´a y Biofı´sica, Instituto de Ciencias Biome´dicas, Facultad de Medicina, Universidad de Chile, Santiago 8380453, ChileIt is generally accepted that during periods of attention to specific stimuli there are changes in the neural activity of central auditorystructures; however, it is controversial whether attention can modulate auditory responses at the cochlear level. Several studies per-formed in animals as well as in humans have attempted to find a modulation of cochlear responses during visual attention with contra-dictory results. Here, we have appraised cochlear sensitivity in behaving chinchillas by measuring, with a chronically implanted round-window electrode, sound-evoked auditory-nerve compound action potentials and cochlear microphonics, a measure of outer hair cellfunction, during selective attention to visual stimuli. Chinchillas were trained in a visual discrimination or in an auditory frequencydiscrimination two-choice task. We found a significant decrease of cochlear sensitivity during the period of attention to visual stimuli inthe animals performing the visual discrimination task, but not in those performing the auditory task, demonstrating that this physio-logical effect is related to selective attention to visual stimuli rather than to an increment in arousal level. Furthermore, the magnitude ofthe cochlear-sensitivity reductions increased in sessions performed with shorter target-light durations (4 – 0.5 s), suggesting that thiseffect is stronger for higher attentional demands of the task. These results demonstrate that afferent auditory activity is modulated byselective attention as early as at sensory transduction, possibly through activation of olivocochlear efferent fibers.Key words: auditory efferents; olivocochlear; corticofugal; attention; cochlear microphonics; top downIntroductionAttention allows subjects to focus cognitive resources on specificstimuli while ignoring others. Although it is generally acceptedthat during periods of attention there are changes in neural ac-tivity in brain auditory centers (Woldorff et al., 1993; Polley et al.,2006), it is controversial whether attention can modulate audi-tory responses at cochlear levels (Hernandez-Peo´ n et al., 1956;Picton et al., 1971).Studies to assess the effect of cross-modal attention on periph-eral auditory responses in animals as well as in humans haveproduced conflicting results. Hernandez-Peo´ n et al. (1956)showed a reduction in click-evoked potentials recorded from thecochlear nucleus in cats while receiving stimuli of other sensorymodalities. In later experiments, Oatman (1971) found an am-plitude reduction of the auditory-nerve compound action poten-tial (CAP) during periods of visual attention in cats. Similarly, inhumans, the auditory-nerve component of tone-pip-evokedbrainstem potentials and the amplitude of click-evoked oto-acoustic emissions were significantly reduced in subjects wheninstructed to count letters flashed on a screen (Lukas, 1980; Puelet al., 1988). However, other research groups failed to replicatethese findings and attributed the observed decrease in cochlearresponses to head or body movements (Dunlop et al., 1965;Wickelgren, 1968). In humans, paying attention to clicks duringan auditory discrimination task, as opposed to reading a bookand ignoring the clicks, produced no changes in click-evokedauditory nerve responses recorded from the external ear canal,despite a significant enhancement in click-evoked cortical poten-tials (Picton et al., 1971; Picton and Hillyard, 1974). Also, inanother study, no significant changes were observed in evokedotoacoustic emissions recorded in subjects performing the samevisual selective attention task used previously by Lukas (1980)and Puel et al. (1988) (Avan and Bonfils, 1992). Because of thesecontradictory results, the proposition that cochlear sensitivityis reduced during cross-modal attention has remainedcontroversial.In this study, we measured cochlear sensitivity by recordingCAP and cochlear microphonic (CM) potentials from the roundwindow of chinchillas while they performed a visual or an audi-tory two-choice discrimination task. We demonstrated that co-chlear sensitivity is transiently reduced during selective attentionto visual stimuli, probably through activation of olivocochlearefferent fibers. The main technical advantages in our experimen-tal design that could have helped the positive outcome of ourexperiments are as follows: (1) the use of a visual cue that delimitsa short period (a few seconds) of high attentional load beforetarget discrimination, (2) the assessment of sensitivity changes byrecording auditory-nerve CAPs that report larger efferent effectsthan otoacoustic emissions (Puria et al., 1996), (3) the use of around-window electrode that allowed us to measure reliable co-Received Aug. 24, 2006; revised March 9, 2007; accepted March 10, 2007.ThisworkwassupportedbyFondoNacionaldeDesarrolloCientı´ficoyTecnolo´gico1020970,Fundacio´nGuillermoPuelma, Universidad de Chile Grant PG-42-2004, and PhD Scholarship Comisio´n Nacional de Investigacio´n Cientı´ficay Tecnolo´gica to P.H.D. and C.M.H. We thank Mario Ruggero for comments on a previous version of this manuscript,threeunknown reviewers who helped us to improve thismanuscript,and Fernando Vergara for technical assistance.Correspondence should be addressed to Dr. Luis Robles, Programa de Fisiologı´a y Biofı´sica, Instituto de CienciasBiome´dicas, Facultad de Medicina, Universidad de Chile, Casilla 70005 Santiago 7, Chile. E-mail:[email protected]:10.1523/JNEUROSCI.3702-06.2007Copyright © 2007 Society for Neuroscience 0270-6474/07/274146-08$15.00/04146 • The Journal of Neuroscience, April 11, 2007 • 27(15):4146 – 4153chlear potentials with amplitudes of tens to hundreds of micro-volts, in contrast with using an external-ear canal electrode thatrecords potentials in the order of 1␮V (Picton et al., 1971), and(4) sampling and averaging electrical responses with a time reso-lution (500 ms) that made it possible to detect transient modula-tions of cochlear potentials related to selective visual attention.Materials and MethodsSubjects and apparatusAll procedures involving animals were made in accordance with the localcommittee of Bioethics