Unveiling expectancy neuronal coding in the cerebral cortex induced by naturalistic tactile stimuli

Project Information

Expectancy

Grant agreement ID: 702726

DOI

10.3030/702726

Project closed

EC signature date 11 March 2016

Start date 1 March 2017

End date 28 February 2019

Funded under

• EXCELLENT SCIENCE - Marie Skłodowska-Curie Actions

Total cost

€ 173 076,00

EU contribution

€ 173 076,00

Coordinated by

CENTRE NATIONAL DE LA RECHERCHE SCIENTIFIQUE CNRS
France

Periodic Reporting for period 1 - Expectancy (Unveiling expectancy neuronal coding in the cerebral cortex induced by naturalistic tactile stimuli)

Reporting period: 2017-03-01 to 2019-02-28

Summary of the context and overall objectives of the project

We address the problem of how does the brain encode predictable sensory information coming from the environment. The way we suddenly notice the cease of a repetitive noise or how magicians surprise us with the unexpected disappearance of an object reveals our preparedness for incoming stimulus. If we want to understand how we encode and use sensory information, it is of most importance to study sensory representations in combination with our internal representation of the world.

This research lies in the domain of sensory processing and encoding. It aims at understanding the basic coding rules and features of the somatosensory cortical area in order to use it as a model of how we more generally encode and use information. This allows to comprehend better and inform on the general healthy state of the brain in the sensory areas, in order to look for differences or malfunctions in the case of disease. This study is also of great importance in the field of brain machine interfaces as it helps on the understanding of general encoding for the use of proper sensory embodiment of prostheses.

The objective of our project is to find neuronal signatures of expectancy signals in a spatiotemporal predictive manner in a somatosensory cortex. We take advantage of the precisely arranged tactile system of the rodents, the whisker system, and provide a carefully controlled multi-whisker stimulation in a highly predictable manner. The arrangement of whiskers in arcs and rows in the snout of the rat allows us to design a converging pattern of whisker deflections towards a single whisker. We simultaneously look into the associated primary sensory cortex, which is the first cortical area to receive the signal from the stimulation. In this area, called ´barrel cortex´, there is an arrangement of neuronal structures in the form of barrels that match the geometry of the whiskers and receive their corresponding sensory input. We looked for neuronal activity arising during truncated spatiotemporal patterns. These stimulations have an absent deflection in the last part of the stimulus that corresponds to the target whisker associated with the barrel being measured.

Our results show that the neuronal activity in the somatosensory cortex carries information about the expected spatiotemporal patterns of stimulation.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

We worked first on the design of highly predictable and repetitive spatiotemporal patterns of stimulation. A thorough study of the system was first done using rich spatiotemporal stimulus dynamics. We made a detailed characterization of the responses of a large population of single units during multi-whisker stimulations. We obtained the population filters which describe the stimuli eliciting the most neuronal activity in the barrel cortex. These filters were used as the deflection profiles of individual whiskers during the construction of the stimulation patterns used to reveal the expectancy signals.

For the construction of the stimulation protocol, we tested different stimulus trains. We built a long protocol consisting on three stages: a pre-test, a training and a post-test. Test phases contain truncated patterns of stimulation in which the expectancy signals can be revealed only after the training. We also looked for short term effects, by including randomly interleaved truncated tests in 10% of the training stimulus train. Converging spatiotemporal patterns of stimulation were provided in the rostro-caudal axis, which has been shown to elicit the bigger responses on the barrel cortex. The optimal training length was of one hour.

In order to provide the controlled multi-whisker deflections, we calibrated and programmed a dedicated tool, called the Matrix (Jacob et al. 2010). This device allows a micrometrically controlled displacement of the 24 caudal whiskers in the snout of an isoflurane anesthetized rat. We measured simultaneously neuronal activity in the ´barrel cortex´ using multielectrode silicone probes. According to the ‘predictive coding’ theory, different populations of neurons may be encoding predictive signals and error signals in different layers of the cortex. In view of this, we selected a linear configuration containing 64 channels that allow the identification of the layers.

Experiments were done and the data was analyzed separating into multi-units and single unit activity and a more global scale of analysis called ´local field potential´. We found different responses during the training phase and in the test phase. Also, three different timescales were shown to exist. The first one, related with a predictive signal appears in an anticipated manner relative to the missing stimulus. The other two signals are delayed, and they denote either a surprise, or a delayed mismatch, as it is suggested by the early and late timing of the neuronal activity.

These results provided a neuronal premise on which we were able to design a model of the activity of the population of the cells in the targeted barrel of the barrel cortex. By means of simulations of the average neuronal activity of columns of the cortex related specifically with this and neighbor barrels, we aimed at reproducing the measured results. This modeling is on progress and we expect to provide further understanding of the system by means of experimental predictions for future experiments.

Regarding the dissemination of results:

A refereed article was published in Nature Communications 9(1) 2018

Five poster presentations were given in International Conferences:
1. COSYNE. Lisbon, Portugal. Mar 2019
2. Neuralnet GDR. Paris, France. Dec 2018
3. Sfn. San Diego, US. Nov 2018
4. Barrels XXXI. Riverside, US. Nov 2018
5. FENS. Berlin, Germany. Jul 2018
6. Sfn. Washington, US. Nov 2017

Results were also presented in three lectures:
1. Argentina Neuroscience Society Meeting. Córdoba, Argentina. Oct 2018
2. TENSS Summer School. Transylvania, Romania. Jun 2018
3. Barrels XXX. Baltimore, US. Nov 2017

Finally, five invited seminar talks were given:
1.Neuroscience Institute. UC Berkeley. Berkeley, US. Nov 2018
2-5.Institutes IFIByNE, IbioBA, Institute Leloir and IFIBIO. Buenos Aires, Argentina. Oct 2018

Publication of the related results on the framework of this project are planned to appear in the form of a manuscript during the year 2019.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

In this project, we studied in a unique and highly controlled manner the impact of spatiotemporally predictive stimulus on the somatosensory cortex. Our results focused for the first time on the fact that the cortex has a precise geometrical match, between stimulus space and cortical space, to study the effect not only temporally but in a spatiotemporal manner. The results are expected to be of general relevance to the neuroscience community both experimentally and theoretically. In particular, the understanding of the encoding of expectancy signals will help the advances that are ongoing in the technological domain that aims at replacing, enhancing or embodying the sensory signals in a brain machine interface. We also expect that future studies will use our findings and our detailed description of the neuronal activity arising from an unexpected stimulus as a grounding reference when studying abnormal neuronal activity in the unhealthy brain. Theoretically, the description of units encoding expectancy signals, can help the community to understand how we generally encode and perceive the world in relation to our inner representation of it.

Rostro Caudal patterns at 2 ms ISI build an advanced, a late and a very late expectancy signal.