Human posterior auditory cortex gates novel sounds to consciousness

Abstract

Life or death in hostile environments depends crucially on one's ability to detect and gate novel sounds to awareness, such as that of a twig cracking under the paw of a stalking predator in a noisy jungle. Two distinct auditory cortex processes have been thought to underlie this phenomenon: (i) attenuation of the so-called N1 response with repeated stimulation and (ii) elicitation of a mismatch negativity response (MMN) by changes in repetitive aspects of auditory stimulation. This division has been based on previous studies suggesting that, unlike for the N1, repetitive "standard" stimuli preceding a physically different "novel" stimulus constitute a prerequisite to MMN elicitation, and that the source loci of MMN and N1 are different. Contradicting these findings, our combined electromagnetic, hemodynamic, and psychophysical data indicate that the MMN is generated as a result of differential adaptation of anterior and posterior auditory cortex N1 sources by preceding auditory stimulation. Early ( approximately 85 ms) neural activity within posterior auditory cortex is adapted as sound novelty decreases. This alters the center of gravity of electromagnetic N1 source activity, creating an illusory difference between N1 and MMN source loci when estimated by using equivalent current dipole fits. Further, our electroencephalography data show a robust MMN after a single standard event when the interval between two consecutive novel sounds is kept invariant. Our converging findings suggest that transient adaptation of feature-specific neurons within human posterior auditory cortex filters superfluous sounds from entering one's awareness.

Fig. 1.

MMN to a novel stimulus presented after a single standard stimulus. (Upper Left) The experimental paradigm. (Upper Right) The mean (±SEM) MMN peak latencies and amplitudes in the different stimulus conditions (n = 7). Peak latencies were shorter, and amplitudes larger, with larger standard-novel sound difference, thus replicating previous observations (5). (Lower) Grand-average subtraction waveforms showing the MMN to 1,320-Hz novel tones at frontal EEG leads. Tentatively, the slight between-condition differences in the responses suggest that repeated stimulus presentation may enhance stimulus-specific adaptation, as reflected in longer latencies and diminished response amplitudes. [Note that to correct for possible baseline shifts, the MMN amplitude was, conservatively, quantified (at Fz) as the difference between the negative-going peak and the average of the preceding and subsequent positive-going peaks. Without this highly conservative correction, somewhat larger MMN amplitudes were observed with a single vs. multiple standard stimuli preceding the novel stimuli.]

Fig. 2.

EEG responses to novel sounds with and without intervening standard stimuli. (Upper Left) A schematic illustration of the stimulus paradigm. (Upper Right) Mean (±SEM) novel sound response latencies and amplitudes in the “novel sounds with standards” and “novel sounds without standards” conditions. (Lower) Grand-averaged (n = 7) novel sound responses in the novel sounds with standards and novel sounds without standards conditions are shown at a frontal (Fz) electrode position. The convergence of response waveforms with the large (four octave) physical difference between the novel sounds and the intervening standard stimuli suggests that the MMN arises because of selective adaptation of the N1 response by preceding standard stimuli, rather than being generated by distinct neural populations.

Fig. 3.

ECD analyses of anterior and posterior auditory cortex N1 responses. (Top) Lateral view of single-subject reconstructed left hemisphere and a patch of inflated cortex [i.e., cortical curvature maps (30)] disclosing auditory areas hidden within the Sylvian fissure. (Middle) Single-subject ECD fits at the novel-response peak latencies show more anterior source loci when the novel sounds are preceded by standard stimuli that are similar in sound frequency. With large (four octave) novel-standard difference this effect disappears. Correspondingly, the amplitude waveforms of the ECDs fitted at response peak latencies converge. (Bottom) Mean (±SEM) amplitudes and latencies of the anterior and posterior N1 responses are shown (n = 7). Notably, the differential adaptation of anterior and posterior N1 responses by preceding standard stimuli may explain the previously observed differences in the single-ECD estimated N1 and MMN source loci (3, 12, 13), by way of altering the center of gravity of the underlying source configuration.

Fig. 4.

The fMRI activations and fMRI-constrained MEG activity (24-26) at anterior and posterior N1 response latencies in the novel sounds with standards and novel sounds without standards conditions. (Top Left) fMRI data used in the fMRI-constrained MEG estimates. (Top Right) Group mean (±SEM) MRI signal intensity changes in the standard sounds alone, novel sounds alone, and novel sounds with standards sounds conditions. (Middle) fMRI-constrained MEG activity, at the latency of the posterior auditory cortex N1 response extends from HG onto PT, STS, MTG, and posterior STG. Note that the activity in areas posterior to the primary auditory cortex is suppressed as a function of decreasing standard-novel sound frequency separation. (Bottom) The estimated auditory cortex activity at the latency of the temporally lagging anterior N1 response, encompassing areas anterior to the primary auditory cortex (i.e., medial two-thirds of the HG), was relatively little affected as the standard-novel difference decreased.

Fig. 5.

A schematic model illustrating how the human posterior auditory cortex gates novel sounds to awareness. The approximate locations of the anterior and posterior auditory cortex areas are shown. In this model, neurons within the anterior auditory cortex are narrowly tuned, whereas those within the posterior auditory cortex are more broadly tuned, on sound frequency (28). Thus, adaptation caused by preceding auditory stimulation (8-10) encompasses a greater extent of cortex in the posterior than anterior auditory areas, as indicated by gradients of blue. Thus, responses to subsequently presented sounds with relatively low novelty are robustly suppressed within the posterior auditory cortex. In contrast, on presentation of a highly novel sound, unadapted feature-specific neurons are activated within posterior auditory cortex, thus accelerating ensuing stimulus feature processing within the anterior auditory cortex and allowing the novel sound to enter one's awareness. Note that the present studies were limited to investigating MMN responses elicited by changes in sound frequency. The fact that feature-specific neurons tuned on sound duration, intensity, and periodicity have been documented in animal studies suggests that the governing principles of our model could be generalized to explain MMN responses to changes in other stimulus features; however, this remains to be determined in future investigations.