Bidirectional plasticity of cortical pattern recognition and behavioral sensory acuity

Journal name:
Nature Neuroscience
Volume:
15,
Pages:
155–161
Year published:
DOI:
doi:10.1038/nn.2966
Received
Accepted
Published online

Abstract

Learning to adapt to a complex and fluctuating environment requires the ability to adjust neural representations of sensory stimuli. Through pattern completion processes, cortical networks can reconstruct familiar patterns from degraded input patterns, whereas pattern separation processes allow discrimination of even highly overlapping inputs. Here we show that the balance between pattern separation and completion is experience dependent. Rats given extensive training with overlapping complex odorant mixtures showed improved behavioral discrimination ability and enhanced piriform cortical ensemble pattern separation. In contrast, behavioral training to disregard normally detectable differences between overlapping mixtures resulted in impaired piriform cortical ensemble pattern separation (enhanced pattern completion) and impaired discrimination. This bidirectional effect was not found in the olfactory bulb; it may be due to plasticity within olfactory cortex itself. Thus pattern recognition, and the balance between pattern separation and completion, is highly malleable on the basis of task demands and occurs in concert with changes in perceptual performance.

At a glance

Figures

  1. Sensory acuity in the naive rat.
    Figure 1: Sensory acuity in the naive rat.

    (a) Olfactory stimulus morphing: the original stimulus, a complex mixture of ten odorant components (10c, each component symbolized by a letter), was either degraded by the progressive removal of its components (10c–1, 10c–2, ...) or transformed by the replacement of one component by another one (10cR1). (b) Cross-correlation analyses of olfactory bulb (OB) and of aPCX single-unit ensemble responses to the standard 10c mix versus its various morphs. OB mitral/tufted cell ensembles (n = 28 units) showed stable decorrelation across all morphs. aPCX pyramidal cell ensembles (n = 20 units) showed no decorrelation if a single component only was removed; decorrelation appeared only when more components were missing. In contrast, the addition of one single unusual component to the complex mix (10cR1) gave a clear separation of the two patterns. *P < 0.05 or better, decorrelation compared to 10c. (c) A two-alternative forced-choice task was used to evaluate the rat's ability to discriminate the 10c full mixture from its morphed versions. (d) Behavioral performances matched aPCX discrimination capacities. Rats could not detect the removal of a single component (purple), whereas they could easily discriminate mixtures in which a novel component had been introduced (green). *P < 0.05 and ***P < 0.001 for each group versus the respective reference performance (vanilla/mint). Error bars, s.e.m.

  2. Learned enhancement in sensory acuity.
    Figure 2: Learned enhancement in sensory acuity.

    (a) After extended training, rats were able to acquire the difficult (10c/10c–1) discrimination; the easy replacement detection performance was reproduced with different animals to match a similar period of training. *P < 0.05, **P < 0.01, ***P < 0.001 versus the reference performance (vanilla/mint). (be) Electrophysiological recordings were performed after rats had reached criterion in the odor discrimination tasks: easy (replacement) for short (2 d; see Fig. 1d) and long (8 d) training, or difficult (10c–1 component removal). OB, olfactory bulb. (b) Mastering a difficult but not an easy behavioral discrimination task was associated with enhanced pattern separation ability in piriform cortical ensembles, whereas mitral/tufted cell ensembles presented unchanged decorrelations (easy/short, n = 23 aPCX units; easy/long, n = 28 aPCX units; difficult, n = 25 units per structure). Decorrelation *P < 0.05 compared to 10c. (c) Breadth of tuning (entropy) of aPCX and OB neurons in naive and trained rats. In aPCX, the breadth of tuning in difficult but not in easy odor-experienced rats was significantly reduced (cells more selective) compared with that in naive rats (**P < 0.01). The same learning did not change the selectivity of mitral/tufted cells. (d,e) Power modulation of odor-evoked beta (15–35 Hz; d) and gamma (40–80 Hz; e) oscillatory activities after discrimination learning. Mastering the difficult discrimination task was associated with enhanced gamma and beta odor-evoked activity compared to the simple task and naive status. n = 212–296 odor-evoked responses per structure and per experimental group. **P < 0.01 and ***P < 0.001, higher power than in naive rats; °P < 0.05, lower power than in naive rats. (f,g) Long-lasting memory of the difficult discrimination training. (f) Maintenance of the behavioral discrimination after a 2-week break in the training. (g) Maintenance of aPCX neurons pattern separation ability after a 2-week break in the training, either without behavioral retrieval test (gray, n = 25 cells) or with and without retrieval test (black, n = 35 cells). *P < 0.05 compared to 10c. Data are shown as mean ± s.e.m.

  3. Experience increases cortical pattern completion.
    Figure 3: Experience increases cortical pattern completion.

    (a) Design of the grouping task. In the first phase (discrimination), two odors A and A′ are associated with a reward in opposite ports and the rats' ability to differentiate them is evaluated; in the second phase (grouping), the odors A and A′ are associated to the same rewarded side and the rats' ability to cluster them in opposition to a third odor B is evaluated. (b,c) Behavioral performances detailed for each odor (same color code as in a). The rats were trained to discriminate (D) then group (G) the original 10c stimulus either with a mixture sharing strong similarities (10cR1, b) or with a dissimilar, single odorant (limonene, c). *P < 0.05 and **P < 0.01, lower performance for a given odor compared to day 2 of the discrimination phase. (d) The grouping of two close odors reversed olfactory cortical decorrelation. An enhancement of correlation between the full 10c mix and all its morphed versions was obtained in rats trained to group close stimuli (n = 31 aPCX units). aPCX discrimination capacities of rats trained to group distant stimuli corresponded to those of naive rats (n = 19 aPCX units). The grouping of close odors did not change olfactory bulb (OB) pattern separation ability (n = 24 mitral/tufted cells). *P < 0.05, significant decorrelation compared to 10c. (e) The breadth of tuning of aPCX neurons in rats trained to group close but not distant odors was significantly higher (cells less selective) than that in naive rats (***P < 0.005). Mitral/tufted cells selectivity did not differ from naive rats after the grouping task. (f,g) Power modulation of odor-evoked beta (f) and gamma (g) oscillatory activities associated to grouping learning in aPCX and OB. n = 156–372 odor-evoked responses per structure and per experimental group. ***P < 0.001, higher power than in naive rats; °°P < 0.01 and °°°P < 0.001, lower power than in naive rats. Data are shown as mean ± s.e.m.

  4. Learned enhancement in sensory generalization.
    Figure 4: Learned enhancement in sensory generalization.

    (a) Behavioral training. The rats' discrimination capacity was evaluated again after achievement of the grouping task. A = 10c; A′ = 10cR1 ('close') or limonene ('distant'); B = vanilla. (b) Averaged performances. The rats were poorer at discriminating close odors after training in the grouping task than they were before (*P < 0.05); this impairment was not observed when the grouping task involved distant odors. (c) Detailed performances over time. The error rate of the discrimination session after the grouping task is divided into three consecutive blocks of trials. *P < 0.05, lower performance for the rats trained to group close odors than for those trained to group distant. Data are shown as mean ± s.e.m.

  5. Transient decrease in sensory acuity associated with poor behavioral performance.
    Figure 5: Transient decrease in sensory acuity associated with poor behavioral performance.

    (a) Electrophysiological recordings were performed at the early stage of the difficult task in rats not yet able to perform the 10c/10c–1 discrimination after a short (2 d) training (see Fig. 1d). Cross-correlation analysis for aPCX ensembles showed high correlations between the 10c full mixture and all its morphed versions, whereas olfactory bulb (OB) decorrelation capacities were unaltered by the same experience (n = 21 and 27 aPCX and OB units, respectively). *P < 0.05, decorrelation compared to 10c. (b) The pseudo-conditioned rats never reached the criterion of the reference performance (error rate <0.25 for vanilla/mint) and were merely exposed, without behavioral consequence, to the same pairs of complex mixtures as the conditioned rats. (c) Cross-correlation analysis for aPCX ensembles in the pseudo-conditioned rats (pseudo) submitted to easy-like (n = 27 units) or difficult-like (n = 26 units) discrimination tasks showed significant correlations between the 10c mix and all its morphed versions. (d) Breadth of tuning. Olfactory bulb and aPCX neurons recorded in rats either at the early stage of the difficult discrimination training or pseudo-conditioned showed comparable odor selectivity to those in naive rats. (e,f) Power modulation of odor-evoked beta (e) and gamma (f) oscillatory activities associated to poor behavioral performances. n = 212–285 odor-evoked responses per structure and per experimental group. *P < 0.05, higher power than in naive rats; °P < 0.05, lower power than in naive rats. Data are shown as mean ± s.e.m.

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Affiliations

  1. Emotional Brain Institute, Nathan Kline Institute for Psychiatric Research, Orangeburg, New York, USA.

    • Julie Chapuis &
    • Donald A Wilson
  2. Department of Child & Adolescent Psychiatry, New York University Langone School of Medicine, New York, New York, USA.

    • Julie Chapuis &
    • Donald A Wilson

Contributions

D.A.W. and J.C. designed the research. J.C. collected data. J.C. and D.A.W. analyzed and interpreted data. J.C. and D.A.W. wrote the paper.

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The authors declare no competing financial interests.

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