It has been postulated that selective temporal coordination between neurons and development of functional neuronal assemblies are fundamental for brain function and behavior. Still, there is little ...evidence that functionally relevant coordination emerges preferentially in neuronal assemblies directly controlling behavioral output. We investigated coherence between primary motor cortex and the dorsal striatum as rats learn an abstract operant task. Striking coherence developed between these regions during learning. Interestingly, coherence was selectively increased in cells controlling behavioral output relative to adjacent cells. Furthermore, the temporal offset of these interactions aligned closely with corticostriatal conduction delays, demonstrating highly precise timing. Spikes from either region were followed by a consistent phase in the other, suggesting that network feedback reinforces coherence. Together, these results demonstrate that temporally precise coherence develops during learning specifically in output-relevant neuronal populations and further suggest that correlations in oscillatory activity serve to synchronize widespread brain networks to produce behavior.
•Coherence develops in corticostriatal networks over the course of learning•Coherence is highly specific to cells relevant for behavioral output•Cortical spikes are precisely timed to reach the striatum during peak excitability•Network activity entrains ongoing oscillations, resulting in coherent interactions
Synchronous activity is thought to facilitate selective information transfer between neuronal populations. Koralek et al. show that coherent activity develops in corticostriatal networks during learning, and this coherence is temporally precise and specific to cells relevant for behavioral output.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
We compared two tasks that are widely used in research on mentalizing—false belief stories and animations of rigid geometric shapes that depict social interactions—to investigate whether the neural ...systems that mediate the representation of others' mental states are consistent across these tasks. Whereas false belief stories activated primarily the anterior paracingulate cortex (APC), the posterior cingulate cortex/precuneus (PCC/PC), and the temporo-parietal junction (TPJ)—components of the distributed neural system for theory of mind (ToM)—the social animations activated an extensive region along nearly the full extent of the superior temporal sulcus, including a locus in the posterior superior temporal sulcus (pSTS), as well as the frontal operculum and inferior parietal lobule (IPL)—components of the distributed neural system for action understanding—and the fusiform gyrus. These results suggest that the representation of covert mental states that may predict behavior and the representation of intentions that are implied by perceived actions involve distinct neural systems. These results show that the TPJ and the pSTS play dissociable roles in mentalizing and are parts of different distributed neural systems. Because the social animations do not depict articulated body movements, these results also highlight that the perception of the kinematics of actions is not necessary to activate the mirror neuron system, suggesting that this system plays a general role in the representation of intentions and goals of actions. Furthermore, these results suggest that the fusiform gyrus plays a general role in the representation of visual stimuli that signify agency, independent of visual form.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Brain-machine interfaces are not only promising for neurological applications, but also powerful for investigating neuronal ensemble dynamics during learning. We trained mice to operantly control an ...auditory cursor using spike-related calcium signals recorded with two-photon imaging in motor and somatosensory cortex. Mice rapidly learned to modulate activity in layer 2/3 neurons, evident both across and within sessions. Learning was accompanied by modifications of firing correlations in spatially localized networks at fine scales.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, UILJ, UKNU, UL, UM, UPUK
Animals acquire behaviors through instrumental conditioning. Brain-machine interfaces have used instrumental conditioning to reinforce patterns of neural activity directly, especially in frontal and ...motor cortices, which are a rich source of signals for voluntary action. However, evidence suggests that activity in primary sensory cortices may also reflect internally driven processes, instead of purely encoding antecedent stimuli. Here, we show that rats and mice can learn to produce arbitrary patterns of neural activity in their primary visual cortex to control an auditory cursor and obtain reward. Furthermore, learning was prevented when neurons in the dorsomedial striatum (DMS), which receives input from visual cortex, were optogenetically inhibited, but not during inhibition of nearby neurons in the dorsolateral striatum. After learning, DMS inhibition did not affect production of the rewarded patterns. These data demonstrate that cortico-basal ganglia circuits play a general role in learning to produce cortical activity that leads to desirable outcomes.
•Rodents learn to produce activity patterns in V1 in order to receive a reward•Visual cortex neurons are volitionally modulated in the absence of visual input•Inhibition of DMS impairs learning, but not production of learned patterns•Basal ganglia circuits play a general role in shaping cortical activity
Neely et al. use brain-machine interface training in rodents to demonstrate that neurons in the primary visual cortex can acquire learned modulations in the absence of visual input, and that this form of learning requires participation of the dorsomedial striatum.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
The ability to learn new skills and perfect them with practice applies not only to physical skills but also to abstract skills, like motor planning or neuroprosthetic actions. Although plasticity in ...corticostriatal circuits has been implicated in learning physical skills, it remains unclear if similar circuits or processes are required for abstract skill learning. Here we use a novel behavioural task in rodents to investigate the role of corticostriatal plasticity in abstract skill learning. Rodents learned to control the pitch of an auditory cursor to reach one of two targets by modulating activity in primary motor cortex irrespective of physical movement. Degradation of the relation between action and outcome, as well as sensory-specific devaluation and omission tests, demonstrate that these learned neuroprosthetic actions are intentional and goal-directed, rather than habitual. Striatal neurons change their activity with learning, with more neurons modulating their activity in relation to target-reaching as learning progresses. Concomitantly, strong relations between the activity of neurons in motor cortex and the striatum emerge. Specific deletion of striatal NMDA receptors impairs the development of this corticostriatal plasticity, and disrupts the ability to learn neuroprosthetic skills. These results suggest that corticostriatal plasticity is necessary for abstract skill learning, and that neuroprosthetic movements capitalize on the neural circuitry involved in natural motor learning.
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DOBA, IJS, IZUM, KILJ, KISLJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Sustained dopaminergic and noradrenergic dynamics independently modulate action drive and diversity during exploitative behavior.
The balance between exploiting known actions and exploring ...alternatives is critical for survival and hypothesized to rely on shifts in neuromodulation. We developed a behavioral paradigm to capture exploitative and exploratory states and imaged calcium dynamics in genetically identified dopaminergic and noradrenergic neurons. During exploitative states, characterized by motivated repetition of the same action choice, dopamine neurons in SNc encoding movement vigor showed sustained elevation of basal activity that lasted many seconds. This sustained activity emerged from longer positive responses, which accumulated during exploitative action-reward bouts, and hysteretic dynamics. Conversely, noradrenergic neurons in LC showed sustained inhibition of basal activity due to the accumulation of longer negative responses in LC. Chemogenetic manipulation of these sustained dynamics revealed that dopaminergic activity mediates action drive, whereas noradrenergic activity modulates choice diversity. These data uncover the emergence of sustained neural states in dopaminergic and noradrenergic networks that mediate dissociable aspects of exploitative bouts.
Neurons in the brain form highly complex networks through synaptic connections. Traditionally, functional connectivity between neurons has been explored using methods such as correlations, which do ...not contain any notion of directionality. Recently, an information-theoretic approach based on directed information theory has been proposed as a way to infer the direction of influence. However, it is still unclear whether this new approach provides any additional insight beyond conventional correlation analyses. In this paper, we present a modified procedure for estimating directed information and provide a comparison of results obtained using correlation analyses on both simulated and experimental data. Using physiologically realistic simulations, we demonstrate that directed information can outperform correlation in determining connections between neural spike trains while also providing directionality of the relationship, which cannot be assessed using correlation. Secondly, applying our method to rodent and primate data sets, we demonstrate that directed information can accurately estimate the conduction delay in connections between different brain structures. Moreover, directed information reveals connectivity structures that are not captured by correlations. Hence, directed information provides accurate and novel insights into the functional connectivity of neural ensembles that are applicable to data from neurophysiological studies in awake behaving animals.
A wirelessly powered 0.125 mm 2 65 nm CMOS IC for Brain-Machine Interface applications integrates four 1.5 μW amplifiers (6.5 μVrms input-referred noise with 10 kHz bandwidth) with power conditioning ...and communication circuitry. The multi-node backscatter frequency locks to a wireless interrogator using a frequency-domain multiple access communication scheme. The full system, verified with wirelessly powered in vivo recordings, consumes 10.5 μW and operates at 1 mm range in air with 50 mW transmit power.
Corticostriatal dynamics exhibit gross alterations over the course of natural motor learning, yet little is known about the role they play in neuroprosthetic tasks. We therefore investigated ...interactions between the striatum and primary motor cortex while rats learned to control a brain-machine interface. Striatal firing rates increased greatly from early to late in learning, suggesting that the striatum underlies similar functions in both natural and neuroprosthetic motor learning. In addition, spike-field coherence between neurons in primary motor cortex and local field potentials in the striatum increased greatly in the alpha band in late learning relative to early learning, suggesting the development of functional interactions in corticostriatal networks over the course of learning.
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