Dataset Information

Anticipatory haemodynamic signals in sensory cortex not predicted by local neuronal activity.

ABSTRACT: Haemodynamic signals underlying functional brain imaging (for example, functional magnetic resonance imaging (fMRI)) are assumed to reflect metabolic demand generated by local neuronal activity, with equal increases in haemodynamic signal implying equal increases in the underlying neuronal activity. Few studies have compared neuronal and haemodynamic signals in alert animals to test for this assumed correspondence. Here we present evidence that brings this assumption into question. Using a dual-wavelength optical imaging technique that independently measures cerebral blood volume and oxygenation, continuously, in alert behaving monkeys, we find two distinct components to the haemodynamic signal in the alert animals' primary visual cortex (V1). One component is reliably predictable from neuronal responses generated by visual input. The other component-of almost comparable strength-is a hitherto unknown signal that entrains to task structure independently of visual input or of standard neural predictors of haemodynamics. This latter component shows predictive timing, with increases of cerebral blood volume in anticipation of trial onsets even in darkness. This trial-locked haemodynamic signal could be due to an accompanying V1 arterial pumping mechanism, closely matched in time, with peaks of arterial dilation entrained to predicted trial onsets. These findings (tested in two animals) challenge the current understanding of the link between brain haemodynamics and local neuronal activity. They also suggest the existence of a novel preparatory mechanism in the brain that brings additional arterial blood to cortex in anticipation of expected tasks.

SUBMITTER: Sirotin YB

PROVIDER: S-EPMC2705195 | biostudies-literature | 2009 Jan

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Anticipatory haemodynamic signals in sensory cortex not predicted by local neuronal activity.

Sirotin Yevgeniy B YB Das Aniruddha A

Nature 20090101 7228

Haemodynamic signals underlying functional brain imaging (for example, functional magnetic resonance imaging (fMRI)) are assumed to reflect metabolic demand generated by local neuronal activity, with equal increases in haemodynamic signal implying equal increases in the underlying neuronal activity. Few studies have compared neuronal and haemodynamic signals in alert animals to test for this assumed correspondence. Here we present evidence that brings this assumption into question. Using a dual- ...[more]

PMID: 19158795

Similar Datasets

Project description:Insects and vertebrates harbor specific neurons that encode the animal's head direction (HD) and provide an internal compass for spatial navigation. Each HD cell fires most strongly in one preferred direction. As the animal turns its head, however, HD cells in rat anterodorsal thalamic nucleus (ADN) and other brain areas fire already before their preferred direction is reached, as if the neurons anticipated the future HD. This phenomenon has been explained at a mechanistic level, but a functional interpretation is still missing. To close this gap, we use a computational approach based on the movement statistics of male rats and a simple model for the neural responses within the ADN HD network. Network activity is read out using population vectors in a biologically plausible manner, so that only past spikes are taken into account. We find that anticipatory firing improves the representation of the present HD by reducing the motion-induced temporal bias inherent in causal decoding. The amount of anticipation observed in ADN enhances the precision of the HD compass read-out by up to 40%. More generally, our theoretical framework predicts that neural integration times not only reflect biophysical constraints, but also the statistics of behaviorally relevant stimuli; in particular, anticipatory tuning should be found wherever neurons encode sensory signals that change gradually in time.SIGNIFICANCE STATEMENT Across different brain regions, populations of noisy neurons encode dynamically changing stimuli. Decoding a time-varying stimulus from the population response involves a trade-off: For short read-out times, stimulus estimates are unreliable as the number of stochastic spikes is small; for long read-outs, estimates are biased because they lag behind the true stimulus. We show that optimal decoding of temporally correlated stimuli not only relies on finding the right read-out time window but requires neurons to anticipate future stimulus values. We apply this general framework to the rodent head-direction system and show that the experimentally observed anticipation of future head directions can be explained at a quantitative level from the neuronal tuning properties, network size, and the animal's head-movement statistics.

Project description:Traumatic brain injury (TBI), caused by direct blows to the head or inertial forces during relative head-brain movement, can result in long-lasting cognitive and motor deficits which can be particularly consequential when they occur in young people with a long life ahead. Much is known of the molecular and anatomical changes produced in TBI but much less is known of the consequences of these changes to neuronal functionality, especially in the cortex. Given that much of our interior and exterior lives are dependent on responsiveness to information from and about the world around us, we have hypothesized that a significant contributor to the cognitive and motor deficits seen after TBI could be changes in sensory processing. To explore this hypothesis, and to develop a model test system of the changes in neuronal functionality caused by TBI, we have examined neuronal encoding of simple and complex sensory input in the rat's exploratory and discriminative tactile system, the large face macrovibrissae, which feeds to the so-called "barrel cortex" of somatosensory cortex. In this review we describe the short-term and long-term changes in the barrel cortex encoding of whisker motion modeling naturalistic whisker movement undertaken by rats engaged in a variety of tasks. We demonstrate that the most common form of TBI results in persistent neuronal hyperexcitation specifically in the upper cortical layers, likely due to changes in inhibition. We describe the types of cortical inhibitory neurons and their roles and how selective effects on some of these could produce the particular forms of neuronal encoding changes described in TBI, and then generalize to compare the effects on inhibition seen in other forms of brain injury. From these findings we make specific predictions as to how non-invasive extra-cranial electrophysiology can be used to provide the high-precision information needed to monitor and understand the temporal evolution of changes in neuronal functionality in humans suffering TBI. Such detailed understanding of the specific changes in an individual patient's cortex can allow for treatment to be tailored to the neuronal changes in that particular patient's brain in TBI, a precision that is currently unavailable with any technique.

Dataset Information

Anticipatory haemodynamic signals in sensory cortex not predicted by local neuronal activity.

Publications

Anticipatory haemodynamic signals in sensory cortex not predicted by local neuronal activity.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets