Jorge L. Armony

Fear conditioning enhances different temporal components of tone-evoked spike trains in auditory cortex and lateral amygdala

Single neurons were recorded in freely behaving rats during fear conditioning from areas of auditory cortex that project to the lateral nucleus of the amygdala (LA). The latency and rate of conditioning and extinction were analyzed, and the results were compared to previous recordings from LA itself. Auditory cortex neurons took more trials to learn, and they responded more slowly than LA neurons within trials. Short-latency plasticity in LA, therefore, reflects inputs from the auditory thalamus rather than the auditory cortex. Unlike LA cells, some auditory cortex cells showed late conditioned responses that seemed to anticipate the unconditioned stimulus, while others showed extinction-resistant memory storage. Thus, rapid conditioning of fear responses to potentially dangerous stimuli depends on plasticity in the amygdala, while cortical areas may be particularly involved in higher cognitive (mnemonic and attentional) processing of fear experiences.

Auditory Processing across the Sleep-Wake Cycle: Simultaneous EEG and fMRI Monitoring in Humans

We combined fMRI and EEG recording to study the neurophysiological responses associated with auditory stimulation across the sleep-wake cycle. We found that presentation of auditory stimuli produces bilateral activation in auditory cortex, thalamus, and caudate during both wakefulness and nonrapid eye movement (NREM) sleep. However, the left parietal and, bilaterally, the prefrontal and cingulate cortices and the thalamus were less activated during NREM sleep compared to wakefulness. These areas may play a role in the further processing of sensory information required to achieve conscious perception during wakefulness. Finally, during NREM sleep, the left amygdala and the left prefrontal cortex were more activated by stimuli having special affective significance than by neutral stimuli. These data suggests that the sleeping brain can process auditory stimuli and detect meaningful events.

How the Brain Processes Emotional Information

In recent years, much progress has been made in elucidating the neural system underlying classic fear conditioning, a well-defined behavioral model of emotional learning and memory processes. (For review, see refs. 1-5.) Although this body of work may not illuminate all aspects of all emotions, it is highly relevant to the emotion “fear” and its various manifestations, including psychopathological manifestations. In fact, the implications of work on fear conditioning have not escaped the attention of researchers who work on a variety of anxiety disorders including phobias, panic, and posttraumatic stress disorder (PTSD). (For reviews, see refs. 2 and 6.) We survey some of the major findings about the neural basis of fear conditioning and discuss some of the broader implications, including those for a neurobiological understanding of PTSD.

Computational modeling of emotion: explorations through the anatomy and physiology of fear conditioning.

Recent discoveries about the neural system and cellular mechanisms in pathways mediating classical fear conditioning have provided a foundation for pursuing concurrent connectionist models of this form of emotional learning. The models described are constrained by the known anatomy underlying the behavior being simulated. To date, implementations capture salient features of fear learning, both at the level of behavior and at the level of single cells, and additionally make use of generic biophysical constraints to mimic fundamental excitatory and inhibitory transmission properties. Owing to the modular nature of the systems model, biophysical modeling can be carried out in a single region, in this case the amygdala. Future directions include application of the biophysical model to questions about temporal summation in the two sensory input paths to amygdala, and modeling of an attentional interrupt signal that will extend the emotional processing model to interactions with cognitive systems.

Emotion processing in the minimally conscious state

As a newly described condition distinct from coma or the vegetative state, minimally conscious state (MCS) is characterised by a threshold level of consciousness, and diagnostic criteria have recently been proposed.1 In MCS, cognitively mediated behaviour occurs inconsistently, but is reproducible or sustained enough to be differentiated from reflexive behaviour. It is clinically essential to distinguish this condition from persistent vegetative state (PVS), due to a potentially more favourable outcome.1 So far, whether patients in MCS can process emotion is unknown. Cortical processing has been described in PVS using auditory and visual functional paradigms with positron emission tomography.2,3 However, to date hardly any functional imaging studies are available in patients in MCS.4 We used fMRI to assess brain activity induced by an emotional stimulus in a patient in MCS. A 17 year old man was riding his bicycle when he was hit by a train. The accident …

GABAA and GABAB receptors differentially regulate synaptic transmission in the auditory thalamo‐amygdala pathway: An in vivo microiontophoretic study and a model

Stimulation of the medial geniculate body elicits extracellular single unit responses in the lateral nucleus of the amygdala that are dependent upon glutamatergic neurotransmission [Li et al. (1995) Exp. Brain Res., 105:87–100]. In the present study, we examined the contribution of inhibitory amino acid transmission to these excitatory responses. Antagonists of GABAA or GABAB receptors were delivered microiontophoretically to cells activated by stimulation of the medial geniculate body. Blockade of GABAA receptors with bicuculline resulted in a pronounced increase in evoked short latency unit responses (4–8 ms). In some cases, cells that were not responsive to the stimulation became responsive in the presence of bicuculline. In contrast, delivery of GABAB antagonists, Phaclofen or 2‐OH‐saclofen, did not affect these short‐latency responses. Using paired‐pulse stimulation, both short (<30 ms) and longer (>50 ms) latency inhibitory processes were revealed. GABAA blockade eliminated the short latency inhibition and GABAB blockade eliminated the longer latency inhibition in most cells. These results suggest that the activation of GABAA and GABAB receptors differentially regulate glutamatergic synaptic transmission in the auditory thalamo‐amygdala pathway. Moreover, our findings suggest that at least part of this regulation is via a feedforward mechanism. We tested the sufficiency of feedforward inhibition to account for the data using a simple computational model that incorporates the results presented here.

Own-sex effects in emotional memory for faces.

The amygdala is known to be critical for the enhancement of memory for emotional, especially negative, material. Importantly, some researchers have suggested a sex-specific hemispheric lateralization in this process. In the case of facial expressions, another important factor that could influence memory success is the sex of the face, which could interact with the emotion depicted as well as with the sex of the perceiver. Whether this is the case remains unknown, as all previous studies of sex difference in emotional memory have employed affective pictures. Here we directly explored this question using functional magnetic resonance imaging in a subsequent memory paradigm for facial expressions (fearful, happy and neutral). Consistent with our hypothesis, we found that the hemispheric laterality of the amygdala involvement in successful memory for emotional material was influenced not only by the sex of the subjects, as previously proposed, but also by the sex of the faces being remembered. Namely, the left amygdala was more active for successfully remembered female fearful faces in women, whereas in men the right amygdala was more involved in memory for male fearful faces. These results confirm the existence of sex differences in amygdala lateralization in emotional memory but also demonstrate a subtle relationship between the observer and the stimulus in this process.