Engaging in an auditory task suppresses responses in auditory cortex

Abstract

Although systems that are involved in attentional selection have been studied extensively, much less is known about nonselective systems. To study these preparatory mechanisms, we compared activity in auditory cortex that was elicited by sounds while rats performed an auditory task ('engaged') with activity that was elicited by identical stimuli while subjects were awake but not performing a task ('passive'). We found that engagement suppressed responses, an effect that was opposite in sign to that elicited by selective attention. In the auditory thalamus, however, engagement enhanced spontaneous firing rates but did not affect evoked responses. These results indicate that neural activity in auditory cortex cannot be viewed simply as a limited resource that is allocated in greater measure as the state of the animal passes from somnolent to passively listening to engaged and attentive. Instead, the engaged condition possesses a characteristic and distinct neural signature in which sound-evoked responses are paradoxically suppressed.

Figure 1. Cortical evoked responses are suppressed in the engaged condition but spontaneous activity is unchanged

(a) Animals implanted with earphones performed a two-alternative choice auditory task (Task 1) for ~30 minutes (engaged period). The animal initiated a trial by poking its nose into the center port. Before and after the engaged period, the ports were blocked and the same stimuli were presented (passive period). (b–d) Examples of single unit, multi-unit and LFP responses elicited by the first stimulus (grey bar) showing suppression in engaged relative to passive condition. Fig. e–h, f–i and g–j show population responses of single units, multiunits and LFP respectively. (e–g) Scatterplot comparing passive and engaged activity across the population. (h–j) Modulation index ((Activity_engaged − Activity_passive)/(Activity_engaged + Activity_passive)) for spontaneous and evoked activity. Because LFP changes were assessed by changes in the stimulus-evoked peak, LFP spontaneous activity was not analyzed in g and j. (* - p<0.05 different from 0; ** - p<0.001 different from 0). Error bars in this and the following figures show s.e.m. For detailed captions, see Supplementary table 1: Experiment summary and SM3: Statistics.

Figure 2. Decision-relevant target is suppressed in engaged condition

(a) Responses evoked by clicks (i.e. task-irrelevant distractors) are attenuated at higher repetition rates in both the engaged (blue) and passive (red) conditions (Task 1). The traces show the average normalized PSTH of cortical multiunit responses (N=60 sites) to six different repetition rates. Line thickness is proportional to s.e.m. (b) Task-dependent suppression (modulation index) of the click-evoked responses decreases at higher stimulation rates. The square and triangle symbols indicate the modulation index for spontaneous firing and the first stimulus, respectively. (c) Example of multiunit cortical response to contralateral task-relevant stimulus. Responses to ipsilateral stimuli were generally weak and were not analyzed. (d–e) The modulation of the target stimulus is correlated with the modulation of the preceding (task-irrelevant) stimulus (d) and has a comparable magnitude (e). (f) Spatial selectivity and task-engaged suppression are statistically uncorrelated (regression line in red in this and following figures), indicating that selective responses were not preferentially enhanced during the task. Spatial selectivity was calculated between the left and right target stimulus during the passive condition. We quantified the spatial selectivity using the absolute selectivity, defined as 2*abs((area under the ROC curve)–0.5) . This quantity is zero if the response was not selective between the left and the right target stimulus and 1 if the response was perfectly selective. (See also Fig. S2: Single unit responses to task relevant and task irrelevant stimuli are equally suppressed during the task).

Figure 3. (a, b) Evoked auditory responses are not suppressed during an auditory task relative to an olfactory task

Animals performed interleaved blocks (~50–70 trials) of an auditory task (engaged-auditory) and an olfactory task (engaged-olfactory). In some experiments (c–f, Task 3) a passive block was also tested. Auditory stimuli (a high and a low tone) were identical in the two (or three) blocks. (a) Example tone-evoked multiunit response in auditory cortex shows no difference between the auditory and olfactory blocks (Task 2). (b) The modulation index ((Activity_{auditory block} − Activity_{olfactory block})/(Activity_{auditory block} + Activity_{olfactory block})) showed no difference between the engaged-auditory and engaged-olfactory conditions (compare engaged vs. passive, Fig. 1; see also SM6: Single unit responses during the intermodal auditory-olfactory task and SM3: Statistics for more detailed figure captions). (c–d) Example PSTH and population data showing that engaged-auditory and engaged-olfactory responses were suppressed relative to the passive condition. (e) There was no significant correlation between frequency selectivity and the (engaged vs. passive) modulation index. Frequency selectivity was calculated during the passive condition between the two pure tone stimulus used as targets We quantified the frequency selectivity using the absolute selectivity, defined as 2*abs((area under the ROC curve)–0.5). This quantity is zero if the response was not selective between the high and the low tone and 1 if the response was perfectly selective. (f) We measured frequency tuning curves at each site (see Fig. S3: Measurement of cortical tuning curves) and found no correlation between the modulation during the task for a particular tone and the distance to the best frequency in octaves.

Figure 4. Changes in arousal and anesthesia have distinct neural signatures

(a–c) Spontaneous but not evoked multiunit responses were suppressed relative to the passive condition during prolonged immobility, possibly associated with sleep. The modulation index was defined as: (Activity_passive − Activity_{prolonged immobility})/(Activity _passive + Activity_{prolonged immobility}). (d–f) Under light anesthesia (ketamine-medetomidine), spontaneous firing rates were also suppressed, and evoked responses were enhanced, relative to the passive condition. The modulation index was defined as: (Activity_passive − Activity_anesthetized)/(Activity_passive + Activity_anesthetized).

Figure 5. Suppression of evoked responses is not caused by self-triggering of stimulus

(a) Head-fixed animals performed a Go/No-Go auditory discrimination task (Task 4). The stimuli started randomly and were not triggered by the subject. Multiunit responses in the engaged-auditory condition were compared with those to the same stimuli presented when the water delivery system was withdrawn (passive). (b–d) Task-engaged suppression of the evoked response was observed, comparable to that seen in Fig 1. (Format parallel to that in Fig. 1. See also Fig. S5: Example and population data showing suppression of sound evoked LFPs in the head-fixed behavior for LFP analysis.)

Figure 6. Neural correlate of engagement differs in auditory thalamus

(a) Thalamic spontaneous responses were elevated in the engaged condition (Task 1) but evoked responses were unchanged. (top) Example multiunit thalamic peri-stimulus time histogram (PSTH). (bottom) Population analysis. (Format parallel to that in Fig. 1; see legend for details).