A Sound-Sensitive Source of Alpha Oscillations in Human Non-Primary Auditory Cortex

Abstract

The functional organization of human auditory cortex can be probed by characterizing responses to various classes of sound at different anatomical locations. Along with histological studies this approach has revealed a primary field in posteromedial Heschl's gyrus (HG) with pronounced induced high-frequency (70–150 Hz) activity and short-latency responses that phase-lock to rapid transient sounds. Low-frequency neural oscillations are also relevant to stimulus processing and information flow, however, their distribution within auditory cortex has not been established. Alpha activity (7–14 Hz) in particular has been associated with processes that may differentially engage earlier versus later levels of the cortical hierarchy, including functional inhibition and the communication of sensory predictions. These theories derive largely from the study of occipitoparietal sources readily detectable in scalp electroencephalography. To characterize the anatomical basis and functional significance of less accessible temporal-lobe alpha activity we analyzed responses to sentences in seven human adults (4 female) with epilepsy who had been implanted with electrodes in superior temporal cortex. In contrast to primary cortex in posteromedial HG, a non-primary field in anterolateral HG was characterized by high spontaneous alpha activity that was strongly suppressed during auditory stimulation. Alpha-power suppression decreased with distance from anterolateral HG throughout superior temporal cortex, and was more pronounced for clear compared to degraded speech. This suppression could not be accounted for solely by a change in the slope of the power spectrum. The differential manifestation and stimulus-sensitivity of alpha oscillations across auditory fields should be accounted for in theories of their generation and function.SIGNIFICANCE STATEMENT To understand how auditory cortex is organized in support of perception, we recorded from patients implanted with electrodes for clinical reasons. This allowed measurement of activity in brain regions at different levels of sensory processing. Oscillations in the alpha range (7–14 Hz) have been associated with functions including sensory prediction and inhibition of regions handling irrelevant information, but their distribution within auditory cortex is not known. A key finding was that these oscillations dominated in one particular non-primary field, anterolateral Heschl's gyrus, and were suppressed when subjects listened to sentences. These results build on our knowledge of the functional organization of auditory cortex and provide anatomical constraints on theories of the generation and function of alpha oscillations.

Target Enhancement or Distractor Suppression? Functionally Distinct Alpha Oscillations form the Basis of Attention

“…In agreement with the view of co-existing mechanisms for target enhancement and distractor suppression (Houghton & Tipper, 1984), a presumably facilitatory effect of low alpha power was observed in regions directly involved in the processing of auditory information (see also Billig et al, 2019), while a potentially suppressive effect of high alpha power was present in motor and frontal regions. What follows from this is that anatomically separate alpha oscillators implement different cognitive functions.…”

Oscillatory correlates of auditory working memory examined with human electrocorticography

“…Non-primary auditory cortex in HGal and STG did not show the same delta power increase as HGpm; indeed power in these regions was more suppressed across low-frequencies (delta-alpha). This distinction between oscillatory signatures in primary and non-primary auditory fields is similar to that observed during active listening to speech (Billig, et al, 2019). In our previous fMRI study (Kumar, et al, 2016), we showed a greater increase in BOLD signal (compared to primary auditory cortex) as we moved up the hierarchy to lateral HG and planum temporale.…”

The generation and propagation of the human alpha rhythm

“…S11). Though there are different sensory alphas in the cortex, our work complements other findings which find broadly similar alpha physiology across areas (39,68,69). However, careful work will need to be done to tease apart how alpha varies between regions.…”