Correction: Representation of foreseeable choice outcomes in orbitofrontal cortex triplet-wise interactions.

[This corrects the article DOI: 10.1371/journal.pcbi.1007862.].

Representation of foreseeable choice outcomes in orbitofrontal cortex triplet-wise interactions.

Shared neuronal variability has been shown to modulate cognitive processing. However, the relationship between shared variability and behavioral performance is heterogeneous and complex in frontal areas such as the orbitofrontal cortex (OFC). Mounting evidence shows that single-units in OFC encode a detailed cognitive map of task-space events, but the existence of a robust neuronal ensemble coding for the predictability of choice outcome is less established. Here, we hypothesize that the coding of foreseeable outcomes is potentially unclear from the analysis of units activity and their pairwise correlations. However, this code might be established more conclusively when higher-order neuronal interactions are mapped to the choice outcome. As a case study, we investigated the trial-to-trial shared variability of neuronal ensemble activity during a two-choice interval-discrimination task in rodent OFC, specifically designed such that a lose-switch strategy is optimal by repeating the rewarded stimulus in the upcoming trial. Results show that correlations among triplets are higher during correct choices with respect to incorrect ones, and that this is sustained during the entire trial. This effect is not observed for pairwise nor for higher than third-order correlations. This scenario is compatible with constellations of up to three interacting units assembled during trials in which the task is performed correctly. More interestingly, a state-space spanned by such constellations shows that only correct outcome states that can be successfully predicted are robust over 100 trials of the task, and thus they can be accurately decoded. However, both incorrect and unpredictable outcome representations were unstable and thus non-decodeable, due to spurious negative correlations. Our results suggest that predictability of successful outcomes, and hence the optimal behavioral strategy, can be mapped out in OFC ensemble states reliable over trials of the task, and revealed by sufficiency complex neuronal interactions.

Variability and information content in auditory cortex spike trains during an interval-discrimination task.

Processing of temporal information is key in auditory processing. In this study, we recorded single-unit activity from rat auditory cortex while they performed an interval-discrimination task. The animals had to decide whether two auditory stimuli were separated by either 150 or 300 ms and nose-poke to the left or to the right accordingly. The spike firing of single neurons in the auditory cortex was then compared in engaged vs. idle brain states. We found that spike firing variability measured with the Fano factor was markedly reduced, not only during stimulation, but also in between stimuli in engaged trials. We next explored if this decrease in variability was associated with an increased information encoding. Our information theory analysis revealed increased information content in auditory responses during engagement compared with idle states, in particular in the responses to task-relevant stimuli. Altogether, we demonstrate that task-engagement significantly modulates coding properties of auditory cortical neurons during an interval-discrimination task.

Cortical auditory adaptation in the awake rat and the role of potassium currents.

Responses to sound in the auditory cortex are influenced by the preceding history of firing. We studied the time course of auditory adaptation in primary auditory cortex (A1) from awake, freely moving rats. Two identical stimuli were delivered with different intervals ranging from 50 ms to 8 s. Single neuron recordings in the awake animal revealed that the response to a sound is influenced by sounds delivered even several seconds earlier, the second one usually yielding a weaker response. To understand the role of neuronal intrinsic properties in this phenomenon, we obtained intracellular recordings from rat A1 neurons in vitro and mimicked the same protocols of adaptation carried out in awake animals by means of depolarizing pulses of identical duration and intervals. The intensity of the pulses was adjusted such that the first pulse would evoke a similar number of spikes as its equivalent in vivo. A1 neurons in vitro adapted with a similar time course but less than in awake animals. At least two potassium currents participated in the in vitro adaptation: a Na(+)-dependent K(+) current and an apamin-sensitive K(+) current. Our results suggest that potassium currents underlie at least part of cortical auditory adaptation during the awake state.

Getting a grip on numbers: numerical magnitude priming in object grasping.

To investigate the functional connection between numerical cognition and action planning, the authors required participants to perform different grasping responses depending on the parity status of Arabic digits. The results show that precision grip actions were initiated faster in response to small numbers, whereas power grips were initiated faster in response to large numbers. Moreover, analyses of the grasping kinematics reveal an enlarged maximum grip aperture in the presence of large numbers. Reaction time effects remained present when controlling for the number of fingers used while grasping but disappeared when participants pointed to the object. The data indicate a priming of size-related motor features by numerals and support the idea that representations of numbers and actions share common cognitive codes within a generalized magnitude system.

Lateral orbitofrontal cortex anticipates choices and integrates prior with current information.

Adaptive behavior requires integrating prior with current information to anticipate upcoming events. Brain structures related to this computation should bring relevant signals from the recent past into the present. Here we report that rats can integrate the most recent prior information with sensory information, thereby improving behavior on a perceptual decision-making task with outcome-dependent past trial history. We find that anticipatory signals in the orbitofrontal cortex about upcoming choice increase over time and are even present before stimulus onset. These neuronal signals also represent the stimulus and relevant second-order combinations of past state variables. The encoding of choice, stimulus and second-order past state variables resides, up to movement onset, in overlapping populations. The neuronal representation of choice before stimulus onset and its build-up once the stimulus is presented suggest that orbitofrontal cortex plays a role in transforming immediate prior and stimulus information into choices using a compact state-space representation.

Slow Modulation of Ongoing Discharge in the Auditory Cortex during an Interval-Discrimination Task.

In this study, we recorded single unit activity from rat auditory cortex while the animals performed an interval-discrimination task. The animals had to decide whether two auditory stimuli were separated by either 150 or 300 ms, and go to the left or right nose poke accordingly. Spontaneous firing in between auditory responses was compared in the attentive versus non-attentive brain states. We describe the firing rate modulation detected during intervals while there was no auditory stimulation. Nearly 18% of neurons (n = 14) showed a prominent neuronal discharge during the interstimulus interval, in the form of an upward or downward ramp towards the second auditory stimulus. These patterns of spontaneous activity were often modulated in the attentive versus passive trials. Modulation of the spontaneous firing rate during the task was observed not only between auditory stimuli, but also in the interval preceding the stimulus. These slow modulatory components could be locally generated or the result of a top-down influence originated in higher associative association areas. Such a neuronal discharge may be related to the computation of the interval time and contribute to the perception of the auditory stimulus.

Coding strategies in number space: memory requirements influence spatial-numerical associations.

The tendency to respond faster with the left hand to relatively small numbers and faster with the right hand to relatively large numbers (spatial numerical association of response codes, SNARC effect) has been interpreted as an automatic association of spatial and numerical information. We investigated in two experiments the impact of task-irrelevant memory representations on this effect. Participants memorized three Arabic digits describing a left-to-right ascending number sequence (e.g., 3-4-5), a descending sequence (e.g., 5-4-3), or a disordered sequence (e.g., 5-3-4) and indicated afterwards the parity status of a centrally presented digit (i.e., 1, 2, 8, or 9) with a left/right keypress response. As indicated by the reaction times, the SNARC effect in the parity task was mediated by the coding requirements of the memory tasks. That is, a SNARC effect was only present after memorizing ascending or disordered number sequences but disappeared after processing descending sequences. Interestingly, the effects of the second task were only present if all sequences within one experimental block had the same type of order. Taken together, our findings are inconsistent with the idea that spatial-numerical associations are the result of an automatic and obligatory cognitive process but do suggest that coding strategies might be responsible for the cognitive link between numbers and space.