Time Scales of Auditory Habituation in the Amygdala and Cerebral Cortex

Habituation is a fundamental form of learning manifested by a decrement of neuronal responses to repeated sensory stimulation. In addition, habituation is also known to occur on the behavioral level, manifested by reduced emotional reactions to repeatedly presented affective stimuli. It is, however, not clear which brain areas show a decline in activity during repeated sensory stimulation on the same time scale as reduced valence and arousal experience and whether these areas can be delineated from other brain areas with habituation effects on faster or slower time scales. These questions were addressed using functional magnetic resonance imaging acquired during repeated stimulation with piano melodies. The magnitude of functional responses in the laterobasal amygdala and in related cortical areas and that of valence and arousal ratings, given after each music presentation, declined in parallel over the experiment. In contrast to this long-term habituation (43 min), short-term decreases occurring within seconds were found in the primary auditory cortex. Sustained responses that remained throughout the whole investigated time period were detected in the ventrolateral prefrontal cortex extending to the dorsal part of the anterior insular cortex. These findings identify an amygdalocortical network that forms the potential basis of affective habituation in human

Anatomical specificity of functional amygdala imaging of responses to stimuli with positive and negative emotional valence

Non-invasive neuroimaging is increasingly used for investigating the human amygdala. Accurate functional localization in the amygdala region is, however, challenging and quantitative data on the anatomical specificity of functional amygdala imaging is lacking. We have therefore retrospectively investigated 114 recently published human functional imaging studies concerned with the amygdala. We determined the anatomical assignment probabilities of a total of 339 reported activation sites to the amygdala defined using a cytoarchitectonically verified probabilistic atlas system. We find that approximately 50% of reported responses were located in the region with high probability (< or =80%) of belonging to the amygdala. This group included responses related both to stimuli of positive and negative emotional valence. Approximately 10% of reported response sites were assigned to the hippocampus, with up to 100% assignment probability. The remaining peaks were either located in the border regions of the amygdala and/or hippocampus or outside of both of these structures. Within the amygdala, the majority of peaks (96.3%) were found in the laterobasal (LB) and superficial (SF) subregions. Only 3.7% of peaks were found in the centromedial group (CM), possibly because anatomically delineating the CM region of the amygdala is particularly difficult and hence its extent might have been underestimated. Moreover, these results show that a core region of the amygdala is responsive to stimuli both of positive and negative emotional valence. The current findings highlight the usefulness of probabilistic amygdala maps and also point to a need for the development of accurate in vivo delineation and parcellation of the amygdala

Functional organization of the human anterior insular cortex

The human insular cortex is involved in a wide range of functions including motor control, language, and homeostatic regulation. Little is known, however, how these functions are topographically organized in the insular cortex and how they are functionally related to the amygdala, which is anatomically connected to the insular cortex. We have investigated these questions by conducting an activation likelihood estimate (ALE) meta-analysis of previously published neuroimaging studies reporting insula effects. We find auditory and language tasks to preferentially activate an area in the dorsal part of the anterior insular cortex (AIC). Motor tasks involving both the upper and lower extremity reproducibly activated a posterior AIC region, adjacent to the sulcus centralis insulae (SCI). Significant co-activation with the probabilistically defined amygdala was located in the ventral AIC where also responses related to peripheral physiological changes were repeatedly reported. These findings show that the human AIC is a functionally differentiated brain region. The dorsal region of the AIC may be involved in auditory-motor integration, while the ventral part of the AIC may interface the amygdala with insular regions involved in the regulation of physiological changes related to emotional states. Thus, the present findings provide insights into the organization of human AIC and a methodological approach that may be further used to refine the emerging functional map of the insular cortex

Illustrates time course of skin conductance responses (SCR, group means).

<p>For this illustration the median (neuroticism score: 1.67) served as the boundary between the high and the low neuroticism groups (please note: in the statistical model neuroticism was used as continuous variable). Five video clip presentations were averaged into one block, i.e. the first block summarizes five video clip presentations that showed laughing infants at the beginning of the fMRI experiment, the following six blocks summarize each five video clip presentations that showed crying children, and finally the last block summarizes five video clip presentations that showed laughing children at the end of the fMRI experiment. Women scoring higher on neuroticism showed overall stronger skin conductance responses to the ongoing exposure to film clips of crying infants. Error bars indicate standard errors.</p

Illustrates significant fMRI blood-oxygen-level dependent (BOLD) signal decline during crying infant (CI) presentations.

<p>Significant response decrements (<i>p</i> < 0.05, FWE-corrected) during CI presentations are shown in purple and rendered on a standard brain surface, (<b>a</b>) the left and (<b>b</b>) right hemisphere. The outline of brain-surface projections of the areas BA44/45 and TE3 from a probabilistic atlas system [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0161181#pone.0161181.ref041" target="_blank">41</a>,<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0161181#pone.0161181.ref042" target="_blank">42</a>] are indicated by black and green lines. <b>(c)</b> to <b>(f)</b>: Significant BOLD signal decline (i.e., habituation) was found in the fusiform gyrus, middle temporal gyrus, TE3 (superior temporal gyrus [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0161181#pone.0161181.ref040" target="_blank">40</a>]), and in the right BA 45. Median percentage of BOLD signal change over the 30 CI presentations for the four example peaks shown in (a) and (b). Error bars indicate standard errors.</p

Significant fMRI blood-oxygen-level dependent (BOLD) signal decline during crying infant presentations.

<p>(<i>p</i> < 0.05 FWE corrected, clustersize clustersize ≥ 15 voxel). IPC = inferior parietal cortex, hOC = human occipital lobe, Te = auditory cortex, EC = entorhinal cortex, SUB = subicular complex, LB = laterobasal amygdala, area 45 = Broca’s homologue, and area 6 = premotor cortex. Peak MNI-coordinates and T-values are given. Anatomical assignments were performed using a probabilistic anatomical atlas system [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0161181#pone.0161181.ref041" target="_blank">41</a>,<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0161181#pone.0161181.ref042" target="_blank">42</a>]</p

Significant fMRI blood-oxygen-level dependent (BOLD) signal for the contrast <i>perception of crying infants > baseline</i> (<i>p</i> < 0.05 FWE corrected, clustersize clustersize ≥ 15 voxel).

<p>Peak MNI-coordinates and T-values are given. Anatomical assignments were performed using a probabilistic anatomical atlas system [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0161181#pone.0161181.ref041" target="_blank">41</a>,<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0161181#pone.0161181.ref042" target="_blank">42</a>].</p

Time scales of auditory habituation in the amygdala and cerebral cortex

Habituation is a fundamental form of learning manifested by a decrement of neuronal responses to repeated sensory stimulation. In addition, habituation is also known to occur on the behavioral level, manifested by reduced emotional reactions to repeatedly presented affective stimuli. It is, however, not clear which brain areas show a decline in activity during repeated sensory stimulation on the same time scale as reduced valence and arousal experience and whether these areas can be delineated from other brain areas with habituation effects on faster or slower time scales. These questions were addressed using functional magnetic resonance imaging acquired during repeated stimulation with piano melodies. The magnitude of functional responses in the laterobasal amygdala and in related cortical areas and that of valence and arousal ratings, given after each music presentation, declined in parallel over the experiment. In contrast to this long-term habituation (43 min), short-term decreases occurring within seconds were found in the primary auditory cortex. Sustained responses that remained throughout the whole investigated time period were detected in the ventrolateral prefrontal cortex extending to the dorsal part of the anterior insular cortex. These findings identify an amygdalocortical network that forms the potential basis of affective habituation in humans