Luis Robles

Evidence shows that selective attention to visual stimuli modulates the gain of cochlear responses, probably through auditory-cortex descending pathways. At the cerebral cortex level, amplitude and phase changes of neural oscillations have been proposed as a correlate of selective attention. However, whether sensory receptors are also influenced by the oscillatory network during attention tasks remains unknown. Here, we searched for oscillatory attention-related activity at the cochlear receptor in humans. We used an alternating visual/auditory selective attention task and measured electroencephalographic activity simultaneously to distortion product otoacoustic emissions (a measure of cochlear receptor-cell activity). In order to search for cochlear oscillatory activity, the otoacoustic emission signal, was included as an additional channel in the electroencephalogram analyses. This method allowed us to study dynamic changes of cochlear oscillations in the same range of frequencies (1-35 Hz) in which cognitive effects are commonly observed in electroencephalogram works. We found the presence of low frequency (<10 Hz) brain and cochlear amplifier oscillations during periods of selective attention to visual and auditory stimuli. Notably, switching between auditory and visual attention modulates the amplitude and the temporal order of brain and inner ear oscillations. These results extend the role of the oscillatory activity network during cognition in neural systems to the receptor level.

There are two types of sensory cells in the mammalian cochlea, inner hair cells, which make synaptic contact with auditory-nerve afferent fibers, and outer hair cells that are innervated by crossed and uncrossed medial olivocochlear (MOC) efferent fibers. Contralateral acoustic stimulation activates the uncrossed efferent MOC fibers reducing cochlear neural responses, thus modifying the input to the central auditory system. The chinchilla, among all studied mammals, displays the lowest percentage of uncrossed MOC fibers raising questions about the strength and frequency distribution of the contralateral-sound effect in this species. On the other hand, MOC effects on cochlear sensitivity have been mainly studied in anesthetized animals and since the MOC-neuron activity depends on the level of anesthesia, it is important to assess the influence of anesthesia in the strength of efferent effects. Seven adult chinchillas (Chinchilla laniger) were chronically implanted with round-window electrodes in both cochleae. We compared the effect of contralateral sound in awake and anesthetized condition. Compound action potentials (CAP) and cochlear microphonics (CM) were measured in the ipsilateral cochlea in response to tones in absence and presence of contralateral sound. Control measurements performed after middle-ear muscles section in one animal discarded any possible middle-ear reflex activation. Contralateral sound produced CAP amplitude reductions in all chinchillas, with suppression effects greater by about 1-3 dB in awake than in anesthetized animals. In contrast, CM amplitude increases of up to 1.9 dB were found in only three awake chinchillas. In both conditions the strongest efferent effects were produced by contralateral tones at frequencies equal or close to those of ipsilateral tones. Contralateral CAP suppressions for 1-6 kHz ipsilateral tones corresponded to a span of uncrossed MOC fiber innervation reaching at least the central third of the chinchilla cochlea

In mammals, efferent projections to the cochlear receptor are constituted by olivocochlear (OC) fibers that originate in the superior olivary complex. Medial and lateral OC neurons make synapses with outer hair cells and with auditory nerve fibers, respectively. In addition to the OC system, there are also descending projections from the auditory cortex that are directed towards the thalamus, inferior colliculus, cochlear nucleus, and superior olivary complex. Olivocochlear function can be assessed by measuring a brainstem reflex mediated by auditory nerve fibers, cochlear nucleus neurons, and OC fibers. Although it is known that the OC reflex is activated by contralateral acoustic stimulation and produces a suppression of cochlear responses, the influence of cortical descending pathways in the OC reflex is largely unknown. Here, we used auditory cortex electrical microstimulation in chinchillas to study a possible cortical modulation of cochlear and auditory nerve responses to tones in the absence and presence of contralateral noise. We found that cortical microstimulation produces two different peripheral modulations: (i) changes in cochlear sensitivity evidenced by amplitude modulation of cochlear microphonics and auditory nerve compound action potentials and (ii) enhancement or suppression of the OC reflex strength as measured by auditory nerve responses, which depended on the intersubject variability of the OC reflex. Moreover, both corticofugal effects were not correlated, suggesting the presence of two functionally different efferent pathways. These results demonstrate that auditory cortex electrical microstimulation independently modulates the OC reflex strength and cochlear sensitivity.

Frequency selectivity is a fundamental cochlear property. Recent studies using otoacoustic emissions and psychophysical forward masking suggest that frequency selectivity is sharper in human than in common laboratory species. This has been disputed based on reports using compound action potentials (CAPs), which reflect activity in the auditory nerve and can be measured in humans. Comparative data of CAPs, obtained with a variety of simultaneous masking protocols, have been interpreted to indicate similarity of frequency tuning across mammals and even birds. Unfortunately, there are several issues with the available CAP measurements which hamper a straightforward comparison across species. We investigate sharpness of CAP tuning in cat and chinchilla using a forward masking notched-noise paradigm—which is less confounded by cochlear nonlinearities than simultaneous masking paradigms and similar to what was used in the psychophysical study reporting sharper tuning in humans. Our parametric study, using different probe frequencies and notch widths, shows relationships consistent with those of auditory nerve fibers (ANFs). The sharpness of tuning, quantified by Q ₁₀ factors, is negatively correlated with probe level and increases with probe frequency, but the Q ₁₀ values are generally lower than the average trend for ANFs. Like the single fiber data, tuning for CAPs is sharper in cat than in chinchilla, but the two species are similar in the dependence of tuning on probe frequency and in the relationship between tuning in ANFs and CAP. Growth-of-maskability functions show slopes <1 indicating that with increasing probe level the probe is more susceptible to cochlear compression than the masker. The results support the use of forward-masked CAPs as an alternative measure to estimate ANF tuning and to compare frequency tuning across species.

The mammalian cochlea has two types of sensory cells; inner hair cells, which receive auditory-nerve afferent innervation, and outer hair cells, innervated by efferent axons of the medial olivocochlear (MOC) system. The role of the MOC system in hearing is still controversial. Recently, by recording cochlear potentials in behaving chinchillas, we suggested that one of the possible functions of the efferent system is to reduce cochlear sensitivity during attention to other sensory modalities (Delano et al. in J Neurosci 27:4146–4153, 2007). However, in spite of these compelling results, the physiological effects of electrical MOC activation on cochlear potentials have not been described in detail in chinchillas. The main objective of the present work was to describe these efferent effects in the chinchilla, comparing them with those in other species and in behavioral experiments. We activated the MOC efferent axons in chinchillas with sectioned middle-ear muscles by applying current pulses at the fourth-ventricle floor. Auditory-nerve compound action potentials (CAP) and cochlear microphonics (CM) were acquired in response to clicks and tones of several frequencies, using a round-window electrode. Electrical efferent stimulation produced CAP amplitude suppressions reaching up to 11 dB. They were higher for low to moderate sound levels. Additionally, CM amplitude increments were found, the largest (≤ 2.5 dB) for low intensity tones. CAP suppression was present at all stimulus frequencies, but was greatest for 2 kHz. CM increments were highest for low-frequency tones, and almost absent at high frequencies. We conclude that the effect obtained in chinchilla is similar to but smaller than that observed in cats, and that the effects seen in awake chinchillas, albeit different in magnitude, are consistent with the activation of efferent fibers.

Twelve rats were trained to perform a two-choice visual detection task in which a right or left light was presented and the animals were required to press the lever located under the illuminated light for a food reward. In seventy percent of the trials the target light was preceded by presentation of a neutral cue (a central light). Relevance of the neutral cue for detection of the target was analyzed by comparing behavioral Indices of attention in its presence and absence. Accuracy was significantly higher in presence than in absence of the neutral cue, while mean response latencies were lower in presence than in absence of the neutral cue. These results indicate that the animals allocated attentional resources on the target detection during a high expectancy period after the onset of the neutral cue. This could facilitate target detection and improve the performance in the presence of the neutral cue.

It is generally accepted that during periods of attention to specific stimuli there are changes in the neural activity of central auditory structures; however, it is controversial whether attention can modulate auditory responses at the cochlear level. Several studies performed in animals as well as in humans have attempted to find a modulation of cochlear responses during visual attention with contradictory 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 cell function, during selective attention to visual stimuli. Chinchillas were trained in a visual discrimination or in an auditory frequency discrimination two-choice task. We found a significant decrease of cochlear sensitivity during the period of attention to visual stimuli in the animals performing the visual discrimination task, but not in those performing the auditory task, demonstrating that this physiological effect is related to selective attention to visual stimuli rather than to an increment in arousal level. Furthermore, the magnitude of the cochlear-sensitivity reductions increased in sessions performed with shorter target-light durations (4–0.5 s), suggesting that this effect is stronger for higher attentional demands of the task. These results demonstrate that afferent auditory activity is modulated by selective attention as early as at sensory transduction, possibly through activation of olivocochlear efferent fibers.

Relevance of a neutral cue for performance in a two-choice visuospatial detection task was examined. Nine rats were trained, 5 with short intertrial interval (ITI) and 4 with long ITI, to detect a target (lateral lights) presented after a neutral-cue (central light). The removal of the neutral-cue decreased accuracy and increased response latencies and omissions. These results demonstrate that a neutral-cue, preceding the target, is relevant for the performance, suggesting that rats are highly expectant during the neutral-cue and reallocate attentional resources during ITI. Furthermore, latencies were higher, omissions were lower and the fall of accuracy was greater for rats with long than with short ITI, which could indicate that the neutral-cue was more relevant for the former group.