Cell assemblies of the basal forebrain Tingley, David; Alexander, Andrew S; Quinn, Laleh K ...
The Journal of neuroscience,
2015-Feb-18, 2015-02-18, 20150218, Letnik:
35, Številka:
7
Journal Article
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The basal forebrain comprises several heterogeneous neuronal subgroupings having modular projection patterns to discrete sets of cortical subregions. Each cortical region forms recurrent projections, ...via prefrontal cortex, that reach the specific basal forebrain subgroups from which they receive afferents. This architecture enables the basal forebrain to selectively modulate cortical responsiveness according to current processing demands. Theoretically, optimal functioning of this distributed network would be enhanced by temporal coordination among coactive basal forebrain neurons, or the emergence of "cell assemblies." The present work demonstrates assembly formation in rat basal forebrain neuronal populations during a selective attention task. Neuron pairs exhibited coactivation patterns organized within beta-frequency time windows (55 ms), regardless of their membership within distinct bursting versus nonbursting basal forebrain subpopulations. Thus, the results reveal a specific temporal framework for integration of information within basal forebrain networks and for the modulation of cortical responsiveness.
Retrosplenial cortex (RSC) is an association cortex supporting spatial navigation and memory. However, critical issues remain concerning the forms by which its ensemble spiking patterns register ...spatial relationships that are difficult for experimental techniques to fully address. We therefore applied an evolutionary algorithmic optimization technique to create spiking neural network models that matched electrophysiologically observed spiking dynamics in rat RSC neuronal ensembles. Virtual experiments conducted on the evolved networks revealed a mixed selectivity coding capability that was not built into the optimization method, but instead emerged as a consequence of replicating biological firing patterns. The experiments reveal several important outcomes of mixed selectivity that may subserve flexible navigation and spatial representation: (a) robustness to loss of specific inputs, (b) immediate and stable encoding of novel routes and route locations, (c) automatic resolution of input variable conflicts, and (d) dynamic coding that allows rapid adaptation to changing task demands without retraining. These findings suggest that biological retrosplenial cortex can generate unique, first-trial, conjunctive encodings of spatial positions and actions that can be used by downstream brain regions for navigation and path integration. Moreover, these results are consistent with the proposed role for the RSC in the transformation of representations between reference frames and navigation strategy deployment. Finally, the specific modeling framework used for evolving synthetic retrosplenial networks represents an important advance for computational modeling by which synthetic neural networks can encapsulate, describe, and predict the behavior of neural circuits at multiple levels of function.
Hippocampal CA1 neuronal ensembles generate sequential patterns of firing activity that contribute to episodic memory formation and spatial cognition. Here we used in vivo calcium imaging to record ...neural ensemble activities in mouse hippocampal CA1 and identified CA1 excitatory neuron sub-populations whose members are active across the same second-long period of time. We identified groups of hippocampal neurons sharing temporally correlated neural calcium activity during behavioral exploration and found that they also organized as clusters in anatomical space. Such clusters vary in membership and activity dynamics with respect to movement in different environments, but also appear during immobility in the dark suggesting an internal dynamic. The strong covariance between dynamics and anatomical location within the CA1 sub-region reveals a previously unrecognized form of topographic representation in hippocampus that may guide generation of hippocampal sequences across time and therefore organize the content of episodic memory.
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•Temporally correlated CA1 pyramidal cells are organized into anatomical clusters•Ensemble activities of intra-cluster cells cover different regions of environment•Anatomical clusters reorganize during obvious environment change•Anatomical clusters continue to exist during immobility in a dark environment
Neuroscience; Molecular neuroscience; Cellular neuroscience
Cortically projecting basal forebrain neurons play a critical role in learning and attention, and their degeneration accompanies age-related impairments in cognition. Despite the impressive ...anatomical and cell-type complexity of this system, currently available data suggest that basal forebrain neurons lack complexity in their response fields, with activity primarily reflecting only macro-level brain states such as sleep and wake, onset of relevant stimuli and/or reward obtainment. The current study examined the spiking activity of basal forebrain neuron populations across multiple phases of a selective attention task, addressing, in particular, the issue of complexity in ensemble firing patterns across time. Clustering techniques applied to the full population revealed a large number of distinct categories of task-phase-specific activity patterns. Unique population firing-rate vectors defined each task phase and most categories of task-phase-specific firing had counterparts with opposing firing patterns. An analogous set of task-phase-specific firing patterns was also observed in a population of posterior parietal cortex neurons. Thus, consistent with the known anatomical complexity, basal forebrain population dynamics are capable of differentially modulating their cortical targets according to the unique sets of environmental stimuli, motor requirements, and cognitive processes associated with different task phases.
Self-motion information influences spatially-specific firing patterns exhibited by hippocampal neurons. Moreover, these firing patterns can repeat across similar subsegments of an environment, ...provided that there is similarity of path shape and head orientations across subsegments. The influence of self-motion variables on repeating fields remains to be determined. To investigate the role of path shape and angular rotation on hippocampal activity, we recorded the activity of CA1 neurons from rats trained to run on spiral-shaped tracks. During inbound traversals of circular-spiral tracks, angular velocity increases continuously. Under this condition, most neurons (74%) exhibited repeating fields across at least three adjacent loops. Of these neurons, 86% exhibited forward shifts in the angles of field centers relative to centers on preceding loops. Shifts were absent on squared-spiral tracks, minimal and less reliable on concentric-circle tracks, and absent on outward-bound runs on circular-spiral tracks. However, outward-bound runs on the circular-spiral track in the dark were associated with backward shifts. Together, the most parsimonious interpretation of the results is that continuous increases or decreases in angular velocity are particularly effective at shifting the center of mass of repeating fields, although it is also possible that a nonlinear integration of step counts contributes to the shift. Furthermore, the unexpected absence of field shifts during outward journeys in light (but not darkness) suggests visual cues around the goal location anchored the map of space to an allocentric reference frame.
Physiological studies suggest spatial representation gradients along the CA1 proximodistal axis. To determine the underlying anatomical basis, we quantitatively mapped canonical and noncanonical ...inputs to excitatory neurons in dorsal hippocampal CA1 along the proximal-distal axis in mice of both sexes using monosynaptic rabies tracing. Our quantitative analyses show comparable strength of subiculum complex and entorhinal cortex (EC) inputs to CA1, significant inputs from presubiculum and parasubiculum to CA1, and a threefold stronger input to proximal versus distal CA1 from CA3. Noncanonical subicular complex inputs exhibit opposing topographic connectivity gradients whereby the subiculum-CA1 input strength systematically increases but the presubiculum-CA1 input strength decreases along the proximal-distal axis. The subiculum input strength cotracks that of the lateral EC, known to be less spatially selective than the medial EC. The functional significance of this organization is verified physiologically for subiculum-to-CA1 inputs. These results reveal a novel anatomical framework by which to determine the circuit bases for CA1 representations.
The spike discharge of hippocampal excitatory principal cells, also called "place cells," is highly location specific, but the discharge of local inhibitory interneurons is thought to display ...relatively low spatial specificity. Whereas in other brain regions, such as sensory neocortex, the activity of interneurons is often exquisitely stimulus selective and directly determines the responses of neighboring excitatory neurons, the activity of hippocampal interneurons typically lacks the requisite specificity needed to shape the defined structure of principal cell fields. Here we show that hippocampal formation interneurons have "on" fields (abrupt increases in activity) and "off" fields (abrupt decreases in activity) that are associated with the same location-specific informational content, spatial resolution, and dependency on context as the "place fields" of CA1 principal cells. This establishes that interneurons have well-defined place fields, thus having important implications for understanding how the hippocampus represents spatial information.
Extended periods of rest in Drosophila melanogaster resemble mammalian sleep states in that they are characterized by heightened arousal thresholds and specific alterations in gene expression 1, 2. ...Defined as inactivity periods spanning 5 or more min, amounts of this sleep-like state are, as in mammals, sensitive to prior amounts of waking activity, time of day, and pharmacological intervention 1–3. Clearly recognizable changes in the pattern and amount of brain electrical activity accompany changes in motor activity and arousal thresholds originally used to identify mammalian sleeping behavior 4–6. Electroencephalograms (EEGs) and/or local field potentials (LFPs) are now widely used to quantify sleep state amounts and define types of sleep. Thus, slow-wave sleep (SWS) is characterized by EEG spindles and large-amplitude delta-frequency (0–3.5 Hz) waves. Rapid-eye movement (REM) sleep is characterized by irregular gamma-frequency cortical EEG patterns and rhythmic theta-frequency (5–9 Hz) hippocampal EEG activity 7. It is unknown whether rest and activity in Drosophila are associated with distinct electrophysiological correlates. To address this issue, we monitored motor activity levels and recorded LFPs in the medial brain between the mushroom bodies, structures implicated in the modulation of locomotor activity, of Drosophila8. The results indicate that LFPs can be reliably recorded from the brains of awake, moving fruit flies, that targeted genetic manipulations can be used to localize sources of LFP activity, and that brain electrical activity of Drosophila is reliably correlated with activity state.
Learning to ignore irrelevant stimuli is essential to achieving efficient and fluid attention, and serves as the complement to increasing attention to relevant stimuli. The different cholinergic ...(ACh) subsystems within the basal forebrain regulate attention in distinct but complementary ways. ACh projections from the substantia innominata/nucleus basalis region (SI/nBM) to the neocortex are necessary to increase attention to relevant stimuli and have been well studied. Lesser known are ACh projections from the medial septum/vertical limb of the diagonal band (MS/VDB) to the hippocampus and the cingulate that are necessary to reduce attention to irrelevant stimuli. We developed a neural simulation to provide insight into how ACh can decrement attention using this distinct pathway from the MS/VDB. We tested the model in behavioral paradigms that require decremental attention. The model exhibits behavioral effects such as associative learning, latent inhibition, and persisting behavior. Lesioning the MS/VDB disrupts latent inhibition, and drastically increases perseverative behavior. Taken together, the model demonstrates that the ACh decremental pathway is necessary for appropriate learning and attention under dynamic circumstances and suggests a canonical neural architecture for decrementing attention.
There are numerous experience-driven changes in cortical circuitry that correlate with improved performance. Improved motor performance on a reach-to-grasp task in rodents is associated with changes ...in long-term potentiation (LTP), synaptogenesis, and movement representations in primary motor cortex (M1) by training days 3, 7, and 10, respectively. We recorded single-cell activity patterns in M1 during reach-to-grasp training to test how neural-spiking properties change with respect to LTP, synaptogenesis, and motor map changes. We also tested how neural-spiking changes relate directly to improved performance by monitoring muscle activity patterns. We found that signal-to-noise ratios (SNRs) of M1 spiking were significantly improved with practice but only after 7-12 d. Three sources of noise were assessed: signal-dependent noise exemplified by the slope of the relationship between mean spike count and count variance per burst, signal-independent noise exemplified by the offset of this relationship, and background firing rates before and after bursts. Signal-independent noise and pre-burst firing rates were reduced with practice. Early performance gains (days 1-6) were dissociated from SNR improvements, whereas later performance gains (day 7-12) were related directly to the magnitude of improvement in both muscle recruitment reliability and success rates. With training, an increased number of cells exhibited firing rates that were correlated with muscle recruitment patterns, with lags suggesting a primary direction of influence from M1 to muscles. These results suggest a functional linkage from local synaptogenesis in M1 to improved spiking reliability of M1 cells to more reliable recruitment of muscles and finally to improved behavioral performance.
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