Hæmodynamic signals underlying functional brain imaging (e.g. fMRI) are assumed to reflect metabolic demand generated by local neuronal activity, with equal increases in hæmodynamic signal implying equal increases in the underlying neuronal activity1-6. Few studies have compared neuronal and hæmodynamic signals in alert animals7,8 to test for this assumed correspondence. Here we present evidence bringing this assumption into question. Using a dual-wavelength optical imaging technique9 that independently measures cerebral blood volume and oxygenation, continuously, in alert behaving monkeys, we find two distinct components to the hæmodynamic 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 independent of visual input or of standard neural predictors of hæmodynamics. This latter component shows predictive timing, with increases of cerebral blood volume in anticipation of trial onsets even in darkness. This trial-locked hæmodynamic 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 2 animals) challenge the current understanding of the link between brain hæmodynamics 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.
In functional brain imaging there is controversy over which hemodynamic signal best represents neural activity. Intrinsic signal optical imaging (ISOI) suggests that the best signal is the early darkening observed at wavelengths absorbed preferentially by deoxyhemoglobin (HbR). It is assumed that this darkening or "initial dip" reports local conversion of oxyhemoglobin (HbO) to HbR, i.e., oxygen consumption caused by local neural activity, thus giving the most specific measure of such activity. The blood volume signal, by contrast, is believed to be more delayed and less specific. Here, we used multiwavelength ISOI to simultaneously map oxygenation and blood volume [i.e., total hemoglobin (HbT)] in primary visual cortex (V1) of the alert macaque. We found that the hemodynamic ''point spread,'' i.e., impulse response to a minimal visual stimulus, was as rapid and retinotopically specific when imaged by using blood volume as when using the initial dip. Quantitative separation of the imaged signal into HbR, HbO, and HbT showed, moreover, that the initial dip was dominated by a fast local increase in HbT, with no increase in HbR. We found only a delayed HbR decrease that was broader in retinotopic spread than HbO or HbT. Further, we show that the multiphasic time course of typical ISOI signals and the strength of the initial dip may reflect the temporal interplay of monophasic HbO, HbR, and HbT signals. Characterizing the hemodynamic response is important for understanding neurovascular coupling and elucidating the physiological basis of imaging techniques such as fMRI.fMRI ͉ imaging ͉ macaque ͉ visual ͉ neurovascular coupling C erebral hemodynamics respond quickly and specifically to local neural activity (1, 2). Hemodynamic signals are thus used extensively as proxies for such activity in functional neuroimaging techniques like fMRI and intrinsic signal optical imaging (ISOI). There has been considerable debate, however, as to which of the possible hemodynamic signals, e.g., changes in local blood oxygenation, volume, or flow, with their distinct response properties, constitutes the ''best'' signal for inferring neural activity (1,(3)(4)(5).The debate regarding the best signal sharpened with reports of initial dips in both ISOI and fMRI signals. ISOI studies consistently found a brief stimulus-evoked darkening followed by a strong brightening at imaging wavelengths preferentially absorbed in deoxyhemoglobin (HbR) [e.g., at 605 nm (6)]. The darkening, later termed the initial dip*, was interpreted as a local conversion of oxyhemoglobin (HbO) to HbR caused by increased oxygen consumption by local neurons before any active vascular response (1, 7) The subsequent brightening was taken to measure the ''rebound'' in [HbO] † caused by a delayed, stimulus-triggered increase in cerebral blood flow (7).In parallel, some fMRI studies reported finding an initial dip before the rise in the blood oxygen level-dependent (BOLD) signal (8). Because the BOLD signal measures changes in [HbR] alone ‡ , the fMRI initial dip was seen a...
When asked to recall the words from a just-presented target list, subjects occasionally recall words that were not on the list. These intrusions either appeared on earlier lists (prior-list intrusions, or PLIs) or had not appeared over the course of the experiment (extra-list intrusions). The authors examined the factors that elicit PLIs in free recall. A reanalysis of earlier studies revealed that PLIs tend to come from semantic associates as well as from recently studied lists, with the rate of PLIs decreasing sharply with list recency. The authors report 3 new experiments in which some items in a given list also appeared on earlier lists. Although repetition enhanced recall of list items, subjects were significantly more likely to make PLIs following the recall of repeated items, suggesting that temporal associations formed in earlier lists can induce recall errors. The authors interpret this finding as evidence for the interacting roles of associative and contextual retrieval processes in recall. Although contextual information helps to focus recall on words in the target list, it does not form an impermeable boundary between current- and prior-list experiences.
We present an extension of the search of associative memory (SAM) model that simulates the effects of both prior semantic knowledge and prior episodic experience on episodic free recall. The model incorporates a memory store for preexisting semantic associations, a contextual drift mechanism, a memory search mechanism that uses both episodic and semantic associations, and a large lexicon including both words from prior lists and unpresented words. These features enabled the model to successfully account for the effects of prior semantic knowledge and prior episodic learning on the pattern of correct recalls and intrusions observed in free recall experiments.
Neuroimaging (for example, functional magnetic resonance imaging) signals are taken as a uniform proxy for local neural activity. By simultaneously recording electrode and neuroimaging (intrinsic optical imaging) signals in alert, task-engaged macaque visual cortex, we recently observed a large anticipatory trial-related neuroimaging signal that was poorly related to local spiking or field potentials. We used these same techniques to study the interactions of this trial-related signal with stimulus-evoked responses over the full range of stimulus intensities, including total darkness. We found that the two signals could be separated, and added linearly over this full range. The stimulus-evoked component was related linearly to local spiking and, consequently, could be used to obtain precise and reliable estimates of local neural activity. The trial-related signal likely has a distinct neural mechanism, however, and failure to account for it properly could lead to substantial errors when estimating local neural spiking from the neuroimaging signal.
During rodent active behavior, multiple orofacial sensorimotor behaviors, including sniffing and whisking, display rhythmicity in the theta range (~5–10 Hz). During specific behaviors, these rhythmic patterns interlock, such that execution of individual motor programs becomes dependent on the state of the others. Here we performed simultaneous recordings of the respiratory cycle and ultrasonic vocalization emission by adult rats and mice in social settings. We used automated analysis to examine the relationship between breathing patterns and vocalization over long time periods. Rat ultrasonic vocalizations (USVs, “50 kHz”) were emitted within stretches of active sniffing (5–10 Hz) and were largely absent during periods of passive breathing (1–4 Hz). Because ultrasound was tightly linked to the exhalation phase, the sniffing cycle segmented vocal production into discrete calls and imposed its theta rhythmicity on their timing. In turn, calls briefly prolonged exhalations, causing an immediate drop in sniffing rate. Similar results were obtained in mice. Our results show that ultrasonic vocalizations are an integral part of the rhythmic orofacial behavioral ensemble. This complex behavioral program is thus involved not only in active sensing but also in the temporal structuring of social communication signals. Many other social signals of mammals, including monkey calls and human speech, show structure in the theta range. Our work points to a mechanism for such structuring in rodent ultrasonic vocalizations.
Stimulus intensity is a fundamental perceptual feature in all sensory systems. In olfaction, perceived odor intensity depends on at least two variables: odor concentration; and duration of the odor exposure or adaptation. To examine how neural activity at early stages of the olfactory system represents features relevant to intensity perception, we studied the responses of mitral/tufted cells (MTCs) while manipulating odor concentration and exposure duration. Temporal profiles of MTC responses to odors changed both as a function of concentration and with adaptation. However, despite the complexity of these responses, adaptation and concentration dependencies behaved similarly. These similarities were visualized by principal component analysis of average population responses and were quantified by discriminant analysis in a trial-by-trial manner. The qualitative functional dependencies of neuronal responses paralleled psychophysics results in humans. We suggest that temporal patterns of MTC responses in the olfactory bulb contribute to an internal perceptual variable: odor intensity.
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