| 1. |
- Enander, Jonas M.D., et al.
(författare)
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A model for self-organization of sensorimotor function : spinal interneuronal integration
- 2022
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Ingår i: Journal of Neurophysiology. - : American Physiological Society. - 0022-3077 .- 1522-1598. ; 127:6, s. 1478-1495
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Tidskriftsartikel (refereegranskat)abstract
- Control of musculoskeletal systems depends on integration of voluntary commands and somatosensory feedback in the complex neural circuits of the spinal cord. It has been suggested that the various connectivity patterns that have been identified experimentally may result from the many transcriptional types that have been observed in spinal interneurons. We ask instead whether the muscle-specific details of observed connectivity patterns can arise as a consequence of Hebbian adaptation during early development, rather than being genetically ordained. We constructed an anatomically simplified model musculoskeletal system with realistic muscles and sensors and connected it to a recurrent, random neuronal network consisting of both excitatory and inhibitory neurons endowed with Hebbian learning rules. We then generated a wide set of randomized muscle twitches typical of those described during fetal development and allowed the network to learn. Multiple simulations consistently resulted in diverse and stable patterns of activity and connectivity that included subsets of the interneurons that were similar to “archetypical” interneurons described in the literature. We also found that such learning led to an increased degree of cooperativity between interneurons when performing larger limb movements on which it had not been trained. Hebbian learning gives rise to rich sets of diverse interneurons whose connectivity reflects the mechanical properties of the system. At least some of the transcriptomic diversity may reflect the effects of this process rather than the cause of the connectivity. Such a learning process seems better suited to respond to the musculoskeletal mutations that underlie the evolution of new species. NEW & NOTEWORTHY We present a model of a self-organizing early spinal cord circuitry, which is attached to a biologically realistic sensorized musculoskeletal system. Without any a priori-defined connectivity or organization, learning induced by spontaneous, fetal-like motor activity results in the emergence of a well-functioning spinal interneuronal circuit whose connectivity patterns resemble in many respects those observed in the adult mammalian spinal cord. Hence, our result questions the importance of genetically controlled wiring for spinal cord function.
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| 2. |
- Enander, Jonas M.D., et al.
(författare)
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A model for self-organization of sensorimotor function : The spinal monosynaptic loop
- 2022
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Ingår i: Journal of Neurophysiology. - : American Physiological Society. - 0022-3077 .- 1522-1598. ; 127:6, s. 1460-1477
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Tidskriftsartikel (refereegranskat)abstract
- Recent spinal cord literature abounds with descriptions of genetic preprogramming and the molecular control of circuit formation. In this paper, we explore to what extent circuit formation based on learning rather than preprogramming could explain the selective formation of the monosynaptic projections between muscle spindle primary afferents and homonymous motoneurons. We adjusted the initially randomized gains in the neural network according to a Hebbian plasticity rule while exercising the model system with spontaneous muscle activity patterns similar to those observed during early fetal development. Normal connectivity patterns developed only when we modeled b motoneurons, which are known to innervate both intrafusal and extrafusal muscle fibers in vertebrate muscles but were not considered in previous literature regarding selective formation of these synapses in animals with paralyzed muscles. It was also helpful to correctly model the greatly reduced contractility of extrafusal muscle fibers during early development. Stronger and more coordinated muscle activity patterns such as observed later during neonatal locomotion impaired projection selectivity. These findings imply a generic functionality of a musculoskeletal system to imprint important aspects of its mechanical dynamics onto a neural network, without specific preprogramming other than setting a critical period for the formation and maturation of this general pattern of connectivity. Such functionality would facilitate the successful evolution of new species with altered musculoskeletal anatomy, and it may help to explain patterns of connectivity and associated reflexes that appear during abnormal development. NEW & NOTEWORTHY A novel model of self-organization of early spinal circuitry based on a biologically realistic plant, sensors, and neuronal plasticity in conjunction with empirical observations of fetal development. Without explicit need for guiding genetic rules, connection matrices emerge that support functional self-organization of the mature pattern of Ia to motoneuron connectivity in the spinal circuitry.
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| 3. |
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| 4. |
- Enander, Jonas M.D., et al.
(författare)
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Ubiquitous neocortical decoding of tactile input patterns
- 2019
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Ingår i: Frontiers in Cellular Neuroscience. - : Frontiers Media SA. - 1662-5102. ; 13
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Tidskriftsartikel (refereegranskat)abstract
- Whereas functional localization historically has been a key concept in neuroscience, direct neuronal recordings show that input of a particular modality can be recorded well outside its primary receiving areas in the neocortex. Here, we wanted to explore if such spatially unbounded inputs potentially contain any information about the quality of the input received. We utilized a recently introduced approach to study the neuronal decoding capacity at a high resolution by delivering a set of electrical, highly reproducible spatiotemporal tactile afferent activation patterns to the skin of the contralateral second digit of the forepaw of the anesthetized rat. Surprisingly, we found that neurons in all areas recorded from, across all cortical depths tested, could decode the tactile input patterns, including neurons of the primary visual cortex. Within both somatosensory and visual cortical areas, the combined decoding accuracy of a population of neurons was higher than for the best performing single neuron within the respective area. Such cooperative decoding indicates that not only did individual neurons decode the input, they also did so by generating responses with different temporal profiles compared to other neurons, which suggests that each neuron could have unique contributions to the tactile information processing. These findings suggest that tactile processing in principle could be globally distributed in the neocortex, possibly for comparison with internal expectations and disambiguation processes relying on other modalities.
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| 5. |
- Etemadi, Leila, et al.
(författare)
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Hippocampal output profoundly impacts the interpretation of tactile input patterns in SI cortical neurons
- 2023
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Ingår i: iScience. - : CELL PRESS. - 2589-0042. ; 26:6
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Tidskriftsartikel (refereegranskat)abstract
- Due to continuous state variations in neocortical circuits, individual somatosensory cortex (SI) neurons in vivo display a variety of intracellular responses to the exact same spatiotemporal tactile input pattern. To manipulate the internal cortical state, we here used brief electrical stimulation of the output region of the hippocampus, which preceded the delivery of specific tactile afferent input patterns to digit 2 of the anesthetized rat. We find that hippocampal output had a diversified, remarkably strong impact on the intracellular response types displayed by each neuron in the primary SI to each given tactile input pattern. Qualitatively, this impact was comparable to that previously described for cortical output, which was surprising given the widely assumed specific roles of the hippocampus, such as in cortical memory formation. The findings show that hippocampal output can profoundly impact the state-dependent interpretation of tactile inputs and hence influence perception, potentially with affective and semantic components.
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| 6. |
- Etemadi, Leila, et al.
(författare)
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Remote cortical perturbation dynamically changes the network solutions to given tactile inputs in neocortical neurons
- 2022
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Ingår i: iScience. - : Elsevier BV. - 2589-0042. ; 25:1
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Tidskriftsartikel (refereegranskat)abstract
- The neocortex has a globally encompassing network structure, which for each given input constrains the possible combinations of neuronal activations across it. Hence, its network contains solutions. But in addition, the cortex has an ever-changing multidimensional internal state, causing each given input to result in a wide range of specific neuronal activations. Here we use intracellular recordings in somatosensory cortex (SI) neurons of anesthetized rats to show that remote, subthreshold intracortical electrical perturbation can impact such constraints on the responses to a set of spatiotemporal tactile input patterns. Whereas each given input pattern normally induces a wide set of preferred response states, when combined with cortical perturbation response states that did not otherwise occur were induced and consequently made other response states less likely. The findings indicate that the physiological network structure can dynamically change as the state of any given cortical region changes, thereby enabling a rich, multifactorial, perceptual capability.
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| 7. |
- Norrlid, Johanna, et al.
(författare)
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Multi-structure Cortical States Deduced From Intracellular Representations of Fixed Tactile Input Patterns
- 2021
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Ingår i: Frontiers in Cellular Neuroscience. - : Frontiers Media SA. - 1662-5102.
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Tidskriftsartikel (refereegranskat)abstract
- The brain has a never-ending internal activity, whose spatiotemporal evolution interacts with external inputs to constrain their impact on brain activity and thereby how we perceive them. We used reproducible touch-related spatiotemporal sensory inputs and recorded intracellularly from rat (Sprague-Dawley, male) neocortical neurons to characterize this interaction. The synaptic responses, or the summed input of the networks connected to the neuron, varied greatly to repeated presentations of the same tactile input pattern delivered to the tip of digit 2. Surprisingly, however, these responses tended to sort into a set of specific time-evolving response types, unique for each neuron. Further, using a set of eight such tactile input patterns, we found each neuron to exhibit a set of specific response types for each input provided. Response types were not determined by the global cortical state, but instead likely depended on the time-varying state of the specific subnetworks connected to each neuron. The fact that some types of responses recurred indicates that the cortical network had a non-continuous landscape of solutions for these tactile inputs. Therefore, our data suggest that sensory inputs combine with the internal dynamics of the brain networks, thereby causing them to fall into one of the multiple possible perceptual attractor states. The neuron-specific instantiations of response types we observed suggest that the subnetworks connected to each neuron represent different components of those attractor states. Our results indicate that the impact of cortical internal states on external inputs is substantially more richly resolvable than previously shown.
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| 8. |
- Oddo, Calogero M., et al.
(författare)
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Artificial spatiotemporal touch inputs reveal complementary decoding in neocortical neurons
- 2017
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Ingår i: Scientific Reports. - : Springer Science and Business Media LLC. - 2045-2322. ; 8
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Tidskriftsartikel (refereegranskat)abstract
- Investigations of the mechanisms of touch perception and decoding has been hampered by difficulties in achieving invariant patterns of skin sensor activation. To obtain reproducible spatiotemporal patterns of activation of sensory afferents, we used an artificial fingertip equipped with an array of neuromorphic sensors. The artificial fingertip was used to transduce real-world haptic stimuli into spatiotemporal patterns of spikes. These spike patterns were delivered to the skin afferents of the second digit of rats via an array of stimulation electrodes. Combined with low-noise intra-and extracellular recordings from neocortical neurons in vivo, this approach provided a previously inaccessible high resolution analysis of the representation of tactile information in the neocortical neuronal circuitry. The results indicate high information content in individual neurons and reveal multiple novel neuronal tactile coding features such as heterogeneous and complementary spatiotemporal input selectivity also between neighboring neurons. Such neuronal heterogeneity and complementariness can potentially support a very high decoding capacity in a limited population of neurons. Our results also indicate a potential neuroprosthetic approach to communicate with the brain at a very high resolution and provide a potential novel solution for evaluating the degree or state of neurological disease in animal models.
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| 9. |
- Rongala, Udaya B., et al.
(författare)
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A Non-spiking Neuron Model With Dynamic Leak to Avoid Instability in Recurrent Networks
- 2021
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Ingår i: Frontiers in Computational Neuroscience. - : Frontiers Media SA. - 1662-5188. ; 15
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Tidskriftsartikel (refereegranskat)abstract
- Recurrent circuitry components are distributed widely within the brain, including both excitatory and inhibitory synaptic connections. Recurrent neuronal networks have potential stability problems, perhaps a predisposition to epilepsy. More generally, instability risks making internal representations of information unreliable. To assess the inherent stability properties of such recurrent networks, we tested a linear summation, non-spiking neuron model with and without a “dynamic leak”, corresponding to the low-pass filtering of synaptic input current by the RC circuit of the biological membrane. We first show that the output of this neuron model, in either of its two forms, follows its input at a higher fidelity than a wide range of spiking neuron models across a range of input frequencies. Then we constructed fully connected recurrent networks with equal numbers of excitatory and inhibitory neurons and randomly distributed weights across all synapses. When the networks were driven by pseudorandom sensory inputs with varying frequency, the recurrent network activity tended to induce high frequency self-amplifying components, sometimes evident as distinct transients, which were not present in the input data. The addition of a dynamic leak based on known membrane properties consistently removed such spurious high frequency noise across all networks. Furthermore, we found that the neuron model with dynamic leak imparts a network stability that seamlessly scales with the size of the network, conduction delays, the input density of the sensory signal and a wide range of synaptic weight distributions. Our findings suggest that neuronal dynamic leak serves the beneficial function of protecting recurrent neuronal circuitry from the self-induction of spurious high frequency signals, thereby permitting the brain to utilize this architectural circuitry component regardless of network size or recurrency.
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| 10. |
- Wahlbom, Anders, et al.
(författare)
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Focal neocortical lesions impair distant neuronal information processing
- 2019
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Ingår i: Journal of Physiology. - 0022-3751. ; 597:16, s. 4357-4371
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Tidskriftsartikel (refereegranskat)abstract
- Key points: Parts of the fields of neuroscience and neurology consider the neocortex to be a functionally parcelled structure. Viewed through such a conceptual filter, there are multiple clinical observations after localized stroke lesions that seem paradoxical. We tested the effect that localized stroke-like lesions have on neuronal information processing in a part of the neocortex that is distant to the lesion using animal experiments. We find that the distant lesion degrades the quality of neuronal information processing of tactile input patterns in primary somatosensory cortex. The findings suggest that even the processing of primary sensory information depends on an intact neocortical network, with the implication that all neocortical processing may rely on widespread interactions across large parts of the cortex. Abstract: Recent clinical studies report a surprisingly weak relationship between the location of cortical brain lesions and the resulting functional deficits. From a neuroscience point of view, such findings raise questions as to what extent functional localization applies in the neocortex and to what extent the functions of different regions depend on the integrity of others. Here we provide an in-depth analysis of the changes in the function of the neocortical neuronal networks after distant focal stroke-like lesions in the anaesthetized rat. Using a recently introduced high resolution analysis of neuronal information processing, consisting of pre-set spatiotemporal patterns of tactile afferent activation against which the neuronal decoding performance can be quantified, we found that stroke-like lesions in distant parts of the cortex significantly degraded the decoding performance of individual neocortical neurons in the primary somatosensory cortex (decoding performance decreased from 30.9% to 24.2% for n = 22 neurons, Wilcoxon signed rank test, P = 0.028). This degrading effect was not due to changes in the firing frequency of the neuron (Wilcoxon signed rank test, P = 0.499) and was stronger the higher the decoding performance of the neuron, indicating a specific impact on the information processing capacity in the cortex. These findings suggest that even primary sensory processing depends on widely distributed cortical networks and could explain observations of focal stroke lesions affecting a large range of functions.
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