Neural activation increases blood flow locally. This vascular signal is used by functional imaging techniques to infer the location and strength of neural activity 1,2 . However, the precise spatial scale over which neural and vascular signals are correlated is unknown. Furthermore, the relative role of synaptic and spiking activity in driving hemodynamic signals is controversial [3][4][5][6][7][8][9] . Prior studies recorded local field potentials (LFPs) as a measure of synaptic activity together with spiking activity and low-resolution hemodynamic imaging. Here we used two-photon microscopy to measure sensory-evoked responses of individual blood vessels (dilation, blood velocity) while imaging synaptic and spiking activity in the surrounding tissue using fluorescent glutamate and calcium sensors. In cat primary visual cortex, where neurons are clustered by their preference for stimulus orientation, we discovered new maps for excitatory synaptic activity, which were organized similar to spiking activity but were less selective for stimulus orientation and direction. We generated tuning curves for individual vessel responses for the first time and found that parenchymal vessels in cortical layer 2/3 were orientation selective. Neighboring penetrating arterioles had different orientation preferences. Pial surface arteries in cats, as well as surface arteries and penetrating arterioles in rat visual cortex (where orientation maps do not exist 10 ), responded to visual stimuli but had no orientation selectivity. We integrated synaptic or spiking responses around individual parenchymal vessels in cats and established that the vascular and neural responses had the same orientation preference. However, synaptic and spiking responses were more selective than vascular responses-vessels frequently responded robustly to stimuli that evoked little to no neural activity in the surrounding tissue. Thus, local neural and hemodynamic signals were partly decoupled. Together, these results indicate that intrinsic cortical properties, such as propagation of vascular dilation between neighboring columns, need to be accounted for when decoding hemodynamic signals.To determine how neural activity leads to changes in cerebral blood flow, the hemodynamic responses of individual vessels need to be compared to neural activity in the surrounding tissue 11 . While sensory-evoked responses of individual vessels have been measured in the Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:
We demonstrate that Alexa Fluor 633 hydrazide (Alexa Fluor 633) selectively labels neocortical arteries and arterioles by binding to elastin fibers. We measured sensory stimulus–evoked arteriole dilation dynamics in mouse, rat and cat visual cortex using Alexa Fluor 633 together with neuronal activity using calcium indicators or blood flow using fluorescein dextran. Arteriole dilation decreased fluorescence recorded from immediately underlying neurons, representing a potential artifact during neuronal functional imaging experiments.
Summary Whether the visual system uses a buffer to store image information and the duration of that storage have been debated intensely in recent psychophysical studies. The long phases of stable perception of reversible figures suggest a memory that persists for seconds. But persistence of similar duration has not been found in signals of the visual cortex. Here we show that figure-ground signals in the visual cortex can persist for a second or more after the removal of the figure-ground cues. When new figure-ground information is presented, the signals adjust rapidly, but when a figure display is changed to an ambiguous edge display, the signals decay slowly – a behavior that is characteristic of memory devices. Figure-ground signals represent the layout of objects in a scene, and we propose that a short-term memory for object layout is important in providing continuity of perception in the rapid stream of images flooding our eyes.
We see objects as having continuity even though the retinal image changes frequently. How such continuity is achieved is hard to understand, because neurons in the visual cortex have small receptive fields that are fixed on the retina, which means that a different set of neurons is activated every time the eyes move. Neurons in areas V1 and V2 signal the local features that are currently in their receptive fields and do not show “remapping” when the image moves. However, subsets of neurons in these areas also carry information about global aspects such as figure-ground organization. Here we carried out experiments to find out if figure-ground organization is remapped. We recorded single neurons in macaque V1 and V2 where figure-ground organization is represented by assignment of contours to regions (border ownership). We had previously found that border ownership signals persist when a figure edge is switched to an ambiguous edge by removing the context. We now used this paradigm to see if border ownership transfers when the ambiguous edge is moved across the retina. In the new position, the edge activated a different set of neurons at a different location in cortex. We found that border ownership was transferred to the newly activated neurons. The transfer occurred whether the edge was moved by a saccade or by moving the visual display. Thus, while the contours are coded in retinal coordinates, their assignment to objects is maintained across movements of the retinal image.
In the primary visual cortex of non-rodent mammals, neurons are clustered according to their preference for stimulus features such as orientation [1][2][3][4] , direction [5][6][7] , ocular dominance 8,9 and binocular disparity 9 . Orientation selectivity is the most widely studied feature and a continuous map with a quasi-periodic layout for preferred orientation is present across the entire primary visual cortex 10,11 . Integrating the synaptic, cellular and network contributions that lead to stimulus selective responses in these functional maps requires the hybridization of imaging techniques that span sub-micron to millimeter spatial scales. With conventional intrinsic signal optical imaging, the overall layout of functional maps across the entire surface of the visual cortex can be determined 12 . The development of in vivo two-photon microscopy using calcium sensitive dyes enables one to determine the synaptic input arriving at individual dendritic spines 13 or record activity simultaneously from hundreds of individual neuronal cell bodies 6,14 . Consequently, combining intrinsic signal imaging with the sub-micron spatial resolution of two-photon microscopy offers the possibility of determining exactly which dendritic segments and cells contribute to the micro-domain of any functional map in the neocortex. Here we demonstrate a high-yield method for rapidly obtaining a cortical orientation map and targeting a specific micro-domain in this functional map for labeling neurons with fluorescent dyes in a non-rodent mammal. With the same microscope used for two-photon imaging, we first generate an orientation map using intrinsic signal optical imaging. Then we show how to target a micro-domain of interest using a micropipette loaded with dye to either label a population of neuronal cell bodies or label a single neuron such that dendrites, spines and axons are visible in vivo. Our refinements over previous methods facilitate an examination of neuronal structure-function relationships with sub-cellular resolution in the framework of neocortical functional architectures. Video LinkThe video component of this article can be found at http://www.jove.com/video/50025/ Protocol 1. Surgical Preparation 1. Induce anesthesia and continuously monitor heart rate, end tidal CO 2 , EEG, and temperature. All procedures were approved by the Institutional Animal Care and Use Committee of the Medical University of South Carolina and were based on those we previously published 9,15 . 2. Expose the dorsal surface of the skull by cutting the skin with a scalpel blade. Dissect the connective tissues overlying the bone using a Brudon curette. Clean the bone using cotton tipped applicators and cotton gauze. Apply bone wax (as needed) to the skull, to stop occasional bleeding through small emissary veins. 3. Attach a titanium or stainless steel head plate to the skull (over the region of interest where the craniotomy will be performed) by using dental cement mixed with black paint (see Materials). A rectangular opening in the ce...
An amazing feature of our visual system is the ability to detect and track objects in the stream of continually changing retinal images. Theories have proposed that the system creates temporary internal representations that persist across changing images, providing continuity. But how such representations are formed in the brain is not known. Here we examined the time course of the responses of border-ownership selective neurons in visual cortex to displays that portray object continuity. We found that the neurons signal border-ownership immediately when new objects appear, but when a border that has been assigned to one object is reassigned to another object while the first remains in the display, the initial responses persist. The neurons continue to signal the initial assignment despite the presence of contradicting figure-ground cues. We propose that border-ownership selectivity reflects mechanisms that create object continuity.
Two-photon imaging studies in mouse primary visual cortex (V1) consistently report that around half of the neurons respond to oriented grating stimuli. However, in cats and primates, nearly all neurons respond to such stimuli. Here we show that mouse V1 responsiveness and selectivity strongly depends on neuronal depth. Moving from superficial layer 2 down to layer 4, the percentage of visually responsive neurons nearly doubled, ultimately reaching levels similar to what is seen in other species. Over this span, the amplitude of neuronal responses also doubled. Moreover, stimulus selectivity was also modulated, not only with depth but also with response amplitude. Specifically, we found that orientation and direction selectivity were greater in stronger responding neurons, but orientation selectivity decreased with depth whereas direction selectivity increased. Importantly, these depth-dependent trends were found not just between layer 2/3 and layer 4 but at different depths within layer 2/3 itself. Thus, neuronal depth is an important factor to consider when pooling neurons for population analyses. Furthermore, the inability to drive the majority of cells in superficial layer 2/3 of mouse V1 with grating stimuli indicates that there may be fundamental differences in the micro-circuitry and role of V1 between rodents and other mammals.
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