Auditory Selective Attention Modulates Activation of Human Inferior Colliculus

Abstract

Rinne T, Balk MH, Koistinen S, Autti T, Alho K, Sams M. Auditory selective attention modulates activation of human inferior colliculus. J Neurophysiol 100: 3323-3327, 2008. First published October 15, 2008 doi:10.1152/jn.90607.2008. Selective auditory attention powerfully modulates neural activity in the human auditory cortex (AC). In contrast, the role of attention in subcortical auditory processing is not well established. Here, we used functional MRI (fMRI) to examine activation of the human inferior colliculus (IC) during strictly controlled auditory attention tasks. The IC is an obligatory midbrain nucleus of the ascending auditory pathway with diverse internal and external connections. The IC also receives a massive descending projection from the AC, suggesting that cortical processes affect IC operations. In this study, 21 subjects selectively attended to left-ear or right-ear sounds and ignored sounds delivered to the other ear. IC activations depended on the direction of attention, indicating that auditory processing in the human IC is not only determined by acoustic input but also by the current behavioral goals. I N T R O D U C T I O NThere has been a long-lasting debate on whether attention modulates processing of sounds as early as in the subcortical structures of the auditory pathway (Hernández-Peón et al. 1956;Jane et al. 1965;Lukas 1980;Maison et al. 2001;Michie et al. 1996;Näätänen 1992;Oatman and Anderson 1977;Ryan and Miller 1977). Although functional MRI (fMRI) studies in humans have ascertained that attention has a strong effect on cortical activity elicited by sounds (Grady et al. 1997;Jäncke et al. 1999;Johnson and Zatorre 2006;Petkov et al. 2004;Rinne et al. 2005Rinne et al. , 2007, there is no unambiguous evidence that attention modulates subcortical auditory activity. Here we focus on the bilateral inferior colliculus of the midbrain where the ascending parallel auditory pathways converge before continuing to the auditory cortex (AC) via the thalamus. The inferior colliculus (IC) also receives substantial corticofugal projections from the AC (Winer 2006). The functional significance of the corticofugal pathway is not well understood, but stimulation of cortical neurons has been shown to modulate response properties of IC neurons (Suga and Ma 2003). Because the IC has been implicated in attention in some animal studies (Jane et al. 1965;Ryan and Miller 1977), it is possible that the corticofugal projections serve to mediate attention effects to the IC (Suga and Ma 2003).We presented asynchronous left and right ear broadband noise bursts to our human subjects at a rapid rate (Fig. 1A).Temporal regularity of the noise bursts was manipulated so that there was a distinct pitch difference between the left and right ear sounds (Griffiths et al. 2001). Subjects were required to selectively attend to sounds at the designated ear to detect frequent (about once per second) pitch increases or decreases among the attended sounds and to indicate, by pressing one of the two buttons, the direction of ...

Tinnitus, Diminished Sound-Level Tolerance, and Elevated Auditory Activity in Humans With Clinically Normal Hearing Sensitivity

“…In other words, the elevations in sound-evoked cortical activation that occurred with tinnitus irrespective of SLT might not reflect the tinnitus percept per se but rather reflect attention drawn to the auditory domain by the presence of tinnitus. The absence of tinnitusrelated effects in subcortical centers in our data is consistent with this attention-based hypothesis for the tinnitus-related effects in PAC because attentional state has a far subtler effect on subcortical compared with cortical auditory fMRI activation (Rinne et al 2008).…”

Tuning In to Sound: Frequency-Selective Attentional Filter in Human Primary Auditory Cortex

“…Unilaterally presented sounds are known to induce a significant bilateral fMRI response in human auditory cortex . However modestly, we did observe spatial attention effects in A1 and R; and previous studies have shown spatially-driven attentional modulation in auditory cortex (Rinne et al, 2008. It is possible that spatial attentional modulation would be greater with a task that required more use of spatial information.…”

“…Previous human studies suggest that attention modulates responses in the region of primary auditory cortex (EEG: Hillyard et al, 1973;Woods et al, 1984;Woldorff et al, 1993;MEG: Fujiwara et al, 1998fMRI: Jäncke et al, 1999Rinne et al, 2008;EcoG: Bidet-Caulet et al, 2007) including frequency-specific enhancement (Paltoglou et al, 2009;Oh et al, 2012). Other fMRI studies suggest that attentional modulation occurs predominantly in secondary, and not primary, auditory cortical areas (Petkov et al, 2004;Woods et al, 2009;Woods et al, 2010;Ahveninen et al, 2011).…”

Task-Dependent Activations of Human Auditory Cortex during Pitch Discrimination and Pitch Memory Tasks

“…Several previous functional magnetic resonance imaging (fMRI) studies have shown that activations of human AC are strongly modulated by attention-engaging auditory tasks (Woodruff et al, 1996;Jäncke et al, 1999;Janata et al, 2002;Rinne et al, 2005;Degerman et al, 2006;Rinne et al, 2008;Mayer et al, 2009). The most pronounced attention-related modulations are typically seen in nonprimary parts of AC in the lateral superior temporal gyrus (STG) (Hall et al, 2000;Petkov et al, 2004;Woods et al, 2009).…”