The bipolar valence-arousal model of conscious experience of emotions is prominent in emotion research. In this work, we examine the validity of this model in the context of feelings elicited by visual stimuli. In particular, we examine whether arousal has a unique contribution over bivariate valence (separate measures for pleasure and displeasure) in explaining physiological arousal (electrodermal activity, EDA) and self-reported feelings at the level of item-specific responses across and within individuals. Our results suggest that self-reports of arousal have neither an advantage in predicting EDA nor make a unique contribution when valence is present in the model. Acceptance of the null hypothesis was confirmed with the use of the Bayesian information criterion. Arousal also showed no advantage over valence in predicting global feelings, but demonstrated a small unique component (1.5% to 4% of variance explained). These results have practical implications for both experimental design in the study of emotions and the underlying bases of their conscious experience.

The lateral entorhinal cortex (LEC) is thought to bind sensory events with the environment where they took place. To compare the relative influence of transient events and temporally stable environmental stimuli on the firing of LEC cells, we recorded neuron spiking patterns in the region during blocks of a trace eyeblink conditioning paradigm performed in two environments and with different conditioning stimuli. Firing rates of some neurons were phasically selective for conditioned stimuli in a way that depended on which room the rat was in; nearly all neurons were tonically selective for environments in a way that depended on which stimuli had been presented in those environments. As rats moved from one environment to another, tonic neuron ensemble activity exhibited prospective information about the conditioned stimulus associated with the environment. Thus, the LEC formed phasic and tonic codes for event-environment associations, thereby accurately differentiating multiple experiences with overlapping features.DOI: http://dx.doi.org/10.7554/eLife.28611.001

The hedonic principle maintains that humans strive to maximize pleasant feelings and avoid unpleasant feelings. Surprisingly, and contrary to hedonic logic, previous experiments have demonstrated a relationship between picture viewing time and arousal (activation) but not with valence (pleasure vs. displeasure), suggesting that arousal rather than the hedonic principle accounts for how individuals choose to spend their time. In 2 experiments we investigated the arousal and hedonic principles underlying viewing time behavior while controlling for familiarity with stimuli, picture complexity, and demand characteristics. Under ad libitum conditions of picture viewing, we found strong relationships between viewing time, valence, and facial corrugator electomyographic (EMG) activity with familiar but not novel pictures. Viewing time of novel stimuli was largely associated with arousal and visual complexity. We conclude that only after initial information about the stimulus is gathered, where we choose to spend our time is guided by the hedonic principle.

Prevailing theories posit that the hippocampus rapidly learns stimulus conjunctions during novel experiences, whereas the neocortex learns slowly through subsequent, off-line interaction with the hippocampus. Parallel evidence, however, shows that the medial prefrontal cortex (mPFC, a critical node of the neocortical network supporting long-term memory storage) undergoes rapid modifications of gene expression, synaptic structure, and physiology at the time of encoding.These observations, along with impaired learning with disrupted mPFC, suggest that mPFC neurons may exhibit rapid neural plasticity during novel experiences; however, direct empirical evidence is lacking. We extracellularly recorded action potentials of cells in the prelimbic region of the mPFC, while male rats received a sequence of stimulus presentations for the first time in life. Moment-to-moment tracking of neural ensemble firing patterns revealed that the prelimbic network activity exhibited an abrupt transition within a minute after the first encounter of an aversive but not neutral stimulus. This network-level change was driven by ~15% of neurons that immediately elevated their spontaneous firing rates and developed firing responses to a neutral stimulus preceding the aversive stimulus within a few instances of their pairings. When a new sensory stimulus was paired with the same aversive stimulus, about half of these neurons generalized firing responses to the new stimulus association. Thus, prelimbic neurons are capable of rapidly forming ensemble codes for novel stimulus associations within minutes. This circuit property may enable the mPFC to rapidly detect and selectively encode the central content of novel experiences.

No abstract

Deep brain stimulation (DBS) of the subgenual cingulate gyrus (SCG) has been used to treat patients with treatment-resistant depression. As in humans, DBS applied to the ventromedial prefrontal cortex of rats induces antidepressant-like responses. Physiological interactions between structures that play a role in depression and antidepressant treatment are still unknown. The present study examined the effect of DBS on inter-region communication by measuring the coherence of local field potentials in the rat infralimbic cortex (IL; homologue of the SCG) and one of its major afferents, the ventral hippocampus (VH). Rats received daily IL DBS treatment (100 μA, 90 μs, 130 Hz; 8 h/day). Recordings were conducted in unrestrained, behaving animals on the day before treatment, after 1 and 10 days of treatment, and 10 days stimulation offset. VH-IL coherence in the 2-4 Hz range was reduced in DBS-treated animals compared with shams after 10 days, but not after only 1 day of treatment. No effect of DBS was observed in the 6-10 Hz (theta) range, where coherence was generally high and could be further evoked with a loud auditory stimulus. Finally, coherence was not affected by fluoxetine (10 mg/kg), suggesting that the effects of DBS were not likely mediated by increased serotonin levels. While these data support the hypothesis that DBS disrupts communication between regions important for expectation-based control of emotion, they also suggest that lasting physiological effects require many days of treatment and, furthermore, may be specific to lower-frequency patterns, the nature and scope of which await further investigation.☆ NI, MP and CH designed the experiments; NI and MP performed the experiments; NI analyzed the data; NI, JN, WDH, KT, and CH wrote the paper.

Prevailing theories posit that the hippocampus rapidly learns stimulus conjunctions during novel experiences, whereas the neocortex learns slowly through subsequent, off-line interaction with the hippocampus. Parallel evidence, however, shows that the medial prefrontal cortex (mPFC, a critical node of the neocortical network supporting long-term memory storage) undergoes rapid modifications of gene expression, synaptic structure, and physiology at the time of encoding. These observations, along with impaired learning with disrupted mPFC, suggest that mPFC neurons may exhibit rapid neural plasticity during novel experiences; however, direct empirical evidence is lacking. We extracellularly recorded action potentials of cells in the prelimbic region of the mPFC, while male rats received a sequence of stimulus presentations for the first time in life. Moment-to-moment tracking of neural ensemble firing patterns revealed that the prelimbic network activity exhibited an abrupt transition within a minute after the first encounter of an aversive but not neutral stimulus. This network-level change was driven by ~15% of neurons that immediately elevated their spontaneous firing rates and developed firing responses to a neutral stimulus preceding the aversive stimulus within a few instances of their pairings. When a new sensory stimulus was paired with the same aversive stimulus, about half of these neurons generalized firing responses to the new stimulus association. Thus, prelimbic neurons are capable of rapidly forming ensemble codes for novel stimulus associations within minutes. This circuit property may enable the mPFC to rapidly detect and selectively encode the central content of novel experiences.

Memory retrieval is thought to depend on the reinstatement of cortical memory representations guided by pattern completion processes in the hippocampus. The lateral entorhinal cortex (LEC) is one of the intermediary regions supporting hippocampal-cortical interactions and houses neurons that prospectively signal past events in a familiar environment. To investigate the functional relevance of the activity of the LEC for cortical reinstatement, we pharmacologically inhibited the LEC and examined its impact on the stability of ensemble firing patterns in one of the efferent targets of the LEC, the medial prefrontal cortex (mPFC). When male rats underwent multiple epochs of identical stimulus sequences in the same environment, the mPFC maintained a stable ensemble firing pattern across repetitions, particularly when the sequence included pairings of neutral and aversive stimuli. With LEC inhibition, the mPFC still formed an ensemble pattern that accurately captured stimuli and their associations within each epoch. However, LEC inhibition markedly disrupted its consistency across the epochs by decreasing the proportion of mPFC neurons that stably maintained firing selectivity for stimulus associations. Thus, the LEC stabilizes cortical representations of learned stimulus associations, thereby facilitating the recovery of the original memory trace without generating a new, redundant trace for familiar experiences. Failure of this process might underlie retrieval deficits in conditions associated with degeneration of the LEC, such as normal aging and Alzheimer's disease.