Frontal cortex neuron types categorically encode single decision variables

Hirokawa, Junya; Vaughan, Alexander; Masset, Paul; Ott, Torben; Kepecs, Ádám

doi:10.1038/s41586-019-1816-9

Cited by 174 publications

(241 citation statements)

References 42 publications

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“…Changes in unit coding were widespread along the session and occurred also under stable experimental conditions and stable behavioral responses. In fact, changes in single-unit coding do not necessarily imply changes in population coding, where coding properties might be preserved by redundancies in the ensemble representation (Hirokawa et al, 2019;Narayanan et al, 2005;Puchalla et al, 2005) or within consistent neural trajectories (Enel et al, 2016;Mante et al, 2013). The fact that we observed the same degree of single-unit changes during maintenance and within-session extinction, which imply different cognitive demands, may therefore suggest that these transient representations are an intrinsic feature of prefrontal dynamics, rather than the result of specific cognitive demands.…”

Section: Discussionmentioning

confidence: 72%

Coordinated prefrontal state transition leads extinction of reward-seeking behaviors

Russo

Spanagel

et al. 2020

Preprint

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Extinction learning suppresses conditioned reward responses and is thus fundamental to adapt to changing environmental demands and to control excessive reward seeking. The medial prefrontal cortex (mPFC) monitors and controls conditioned reward responses. Using in vivo multiple single-unit recordings of mPFC we studied the relationship between single-unit and population dynamics during different phases of an operant conditioning task. To examine the fine temporal relation between neural activity and behavior, we developed a model-based statistical analysis that captured behavioral idiosyncrasies. We found that single-unit responses to conditioned stimuli changed throughout the course of a session even under stable experimental conditions and consistent behavior. However, when behavioral responses to task contingencies had to be updated during the extinction phase, unitspecific modulations became coordinated across the whole population, pushing the network into a new stable attractor state. These results show that extinction learning is not associated with suppressed mPFC responses to conditioned stimuli, but is driven by single-unit coordination into population-wide transitions of the animal's internal state.

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Section: Discussionmentioning

confidence: 72%

Coordinated prefrontal state transition leads extinction of reward-seeking behaviors

Russo

Spanagel

et al. 2020

Preprint

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“…Our finding that reward context information is represented preferentially in intracortically-projecting neurons suggests that corticocortical networks are likely a key player underlying maintenance of this activity. While not explicitly tested, our observations may aid in providing a transcriptomic and projection-based cellular context to the body of literature that has linked PFC to working memory (Spellman et al, 2015;Kamigaki and Dan, 2017;Bolkan et al, 2017;Schmitt et al, 2017) and the representation of decision variables such as value (Bari et al, 2019;Hirokawa et al, 2019), both of which could be in play during our uncued task.…”

Section: Distribution Of Task Information Across Brain Regions and Cementioning

confidence: 89%

Differential encoding in prefrontal cortex projection neuron classes across cognitive tasks

Lui

Nguyen

Grutzner

et al. 2020

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Single-cell transcriptomics has been widely applied to classify neurons in the mammalian brain, while systems neuroscience has historically analyzed the encoding properties of cortical neurons without considering cell types. Here we examine how specific transcriptomic types of mouse prefrontal cortex (PFC) projection neurons relate to axonal projections and encoding properties across multiple cognitive tasks. We found that most types projected to multiple targets, and most targets received projections from multiple types, except PFC→PAG (periaqueductal gray). By comparing Ca 2+ -activity of the molecularly homogeneous PFC→PAG type against two heterogeneous classes in several two-alternative choice tasks in freely-moving mice, we found that all task-related signals assayed were qualitatively present in all examined classes. However, PAG-projecting neurons most potently encoded choice in cued tasks, whereas contralateral PFC-projecting neurons most potently encoded reward context in an uncued task. Thus, task signals are organized redundantly, but with clear quantitative biases across cells of specific molecular-anatomical characteristics.

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“…These 41 studies highlight the complex changes occurring in neural responses across 42 epochs of a given task, which can provide orthogonal neural subspaces for 43 independent computations. In contrast, individual neurons in many cortical 44 areas have been shown to often encode relevant information across multiple 45 epochs (Anterior cingulate cortex 10 , Insular cortex 11 , Motor cortex 12 , 46 Orbitofrontal cortex [13][14][15] , and Perirhinal cortex 16 ), suggesting their ability to 47 support coherent representations through different task-epochs. Because of 48 4 the differences in the forms of explanation in these studies (that is, 49 population or single-neuron level), how coherent representations carried by 50 individual neurons can be reconciled with dynamically changing population 51 structure has not been well investigated.…”

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confidence: 99%

Dynamic coordination of the perirhinal cortical neurons supports coherent representations between task epochs

Ohnuki

Osako

Manabe

et al. 2019

Preprint

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13 14 Cortical neurons show distinct firing patterns across multiple task-epochs 15 characterized by distinct computational aspects. Recent studies suggest that 16 such distinct patterns underly dynamic population code achieving 17 computational flexibility, whereas neurons in some cortical areas often show 18 coherent firing patterns across epochs. To understand how such coherent 19 single-neuron code contribute to dynamic population code, we analyzed 20 neural responses in the perirhinal cortex (PRC) during cue and reward 21 epochs of a two-alternative forced-choice task. We found that the PRC 22 neurons often encoded the opposite choice-directions between those epochs. 23 By using principal component analysis as population-level analysis, we 24 identified neural subspaces associated with each epoch, which reflected 25 coordinated patterns across the neurons. The cue and reward epochs shared 26 neural dimensions where the choice directions were consistently 27 discriminated. Interestingly, those dimensions were supported by 28 dynamically changing contributions of individual neurons. These results 29 indicated heterogeneity of coherent single-neuron responses in their 30 3 contribution to population code. 31 32 33 65 two-alternative forced-choice task and analyzed neural responses in two 66 5 epochs, where different computations are demanded: making predictions 67 about the outcome of choices (cue epoch) and reinforcing the choices (reward 68 epoch). By taking advantage of the interleaved visual and olfactory cue 69 stimuli, which allowed us to evaluate modality-independent encodings, we 70 analyzed dynamic population encodings related to different choices during 71 those epochs in relation to single-neuron level selectivity. 72 73 74 Results 75 76Neurons in the PRC encode choice directions during a two-alternative 77 forced-choice task. We trained rats to perform a two-alternative forced-78 choice task where they chose a target port (left/right) associated with a 79 presented cue to obtain reward ( Fig. 1a-b). The task performance was of a 80 similar level regardless of the cue modality (mean correct rate in visual 81 trials = 95.6 ± 5.5%; olfactory trials = 92.3 ± 4.3%). We recorded spiking 82 activities from the left PRC (n = 207 neurons) during the task performance 83 (37 sessions in five rats). 84 6 As shown in Fig. 1c, the PRC neurons typically showed distinct temporal 85 firing patterns in left and right trials. To characterize how the PRC was 86 activated by different trial conditions, we compared firing pattens among 87 different cue-modalities and choices across all the recorded neurons. The 88 neurons were sorted by their peak firing rates in visually-cued left choice 89 trials (top left in Fig. 1d). As consistent with previous studies in other brain 90 regions 28-33 , the peak responses of the PRC neurons tiled the duration of a 91 trial. The response patterns across the neurons were well preserved 92 between the cue modalities but much less so between the choice directions 93 (comparison between th...

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Frontal cortex neuron types categorically encode single decision variables

Cited by 174 publications

References 42 publications

Coordinated prefrontal state transition leads extinction of reward-seeking behaviors

Coordinated prefrontal state transition leads extinction of reward-seeking behaviors

Differential encoding in prefrontal cortex projection neuron classes across cognitive tasks

Dynamic coordination of the perirhinal cortical neurons supports coherent representations between task epochs

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