Behavioral Detection of Electrical Microstimulation in Different Cortical Visual Areas

Murphey, Dona K.; Maunsell, John H. R.

doi:10.1016/j.cub.2007.03.066

Cited by 106 publications

(107 citation statements)

References 48 publications

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“…Within a few days, current detection thresholds decreased from 5-70 A in the first training session to 2-5 A. These values are comparable with the lowest cortical microstimulation detection thresholds found in humans (Schmidt et al, 1996), monkeys (Bartlett and Doty, 1980;de Lafuente and Romo, 2005;Murphey and Maunsell, 2007), and rats (Butovas and Schwarz, 2007;Houweling and Brecht, 2008). Once animals responded consistently to microstimulation currents Յ5 A, we started single-cell stimulation experiments.…”

Section: Resultssupporting

confidence: 53%

Behavioral Detectability of Single-Cell Stimulation in the Ventral Posterior Medial Nucleus of the Thalamus

Voigt¹,

Brecht²,

Houweling³

2008

J. Neurosci.

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In mammals, most sensory information passes through the thalamus before reaching cortex. In the rat whisker system, each macrovibrissa is represented by ϳ250 neurons in the ventral posterior medial nucleus (VPM) of the thalamus and ϳ10,000 neurons in a cortical barrel column. Here we quantify the sensory impact of individual thalamic neurons in the rat VPM. We first trained animals to report microstimulation of VPM. All animals learned to report microstimulation currents of 2-5 A. We then evoked action potentials (APs) in single thalamic neurons close to the microstimulation site using juxtacellular stimulation, adding on average 17.8 APs to 2.6 spontaneous APs during 200 ms current applications. A population analysis revealed that animals responded equally often in single-cell stimulation trials as in catch trials without stimulation, suggesting that APs of single thalamic cells in VPM lead to either no or only a very weak perceptual effect. These results are surprising given the relatively small number of VPM neurons and our previous observations that single neurons in other parts of the vibrissal system do have an impact on perception or motor output. Our findings therefore suggest that neural representations in whisker thalamus are more distributed than in other whisker-related structures.

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Section: Resultssupporting

confidence: 53%

Behavioral Detectability of Single-Cell Stimulation in the Ventral Posterior Medial Nucleus of the Thalamus

Voigt¹,

Brecht²,

Houweling³

2008

J. Neurosci.

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“…S2), as would be expected if the animals were directly detecting changes in neuronal activity and not the laser light. Shorter reaction times to cortical stimulation [∼150 ms minimum compared with ∼210 ms minimum in a visual task (23)] are further evidence that animals detect direct neuronal activation, as has been shown previously in a range of species and brain areas (24)(25)(26)(27)(28).…”

Section: Resultsmentioning

confidence: 82%

Cortical neural populations can guide behavior by integrating inputs linearly, independent of synchrony

Histed

Maunsell

2013

Proc. Natl. Acad. Sci. U.S.A.

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Neurons are sensitive to the relative timing of inputs, both because several inputs must coincide to reach spike threshold and because active dendritic mechanisms can amplify synchronous inputs. To determine if input synchrony can influence behavior, we trained mice to report activation of excitatory neurons in visual cortex using channelrhodopsin-2. We used light pulses that varied in duration from a few milliseconds to 100 ms and measured neuronal responses and animals' detection ability. We found detection performance was well predicted by the total amount of light delivered. Short pulses provided no behavioral advantage, even when they concentrated evoked spikes into an interval a few milliseconds long. Arranging pulses into trains of varying frequency from beta to gamma also produced no behavioral advantage. Light intensities required to drive behavior were low (at low intensities, channelrhodopsin-2 conductance varies linearly with intensity), and the accompanying changes in firing rate were small (over 100 ms, average change: 1.1 spikes per s). Firing rate changes varied linearly with pulse intensity and duration, and behavior was predicted by total spike count independent of temporal arrangement. Thus, animals' detection performance reflected the linear integration of total input over 100 ms. This behavioral linearity despite neurons' nonlinearities can be explained by a population code using noisy neurons. Ongoing background activity creates probabilistic spiking, allowing weak inputs to change spike probability linearly, with little amplification of coincident input. Summing across a population then yields a total spike count that weights inputs equally, regardless of their arrival time.neuronal circuits | population coding | optogenetics | mouse M any neurons in the brain receive thousands of inputs spread over their dendritic trees, and several of those inputs need to be active simultaneously to generate a spike reliably (1, 2). In this way, coincident synaptic inputs can be amplified relative to asynchronous inputs. In addition to this nonlinearity caused by spike threshold, other active processes such as dendritic calcium spikes (3-5) can preferentially amplify synchronous inputs. A variety of ways that timing could impact network function have been explored, including oscillatory synchronization (6, 7), strong cascading effects of individual neurons or synapses (8-11), and information encoding via temporal patterns (12). In the songbird, for example, song neurons receive precisely timed coincident input that recruits active calcium conductances, generating strong, reliable spike bursts that control the song (13, 14). However, synchrony might not always be critical for neuronal processing. Several types of models show that neuronal networks can be insensitive to precise spike timing even though individual neurons are highly sensitive. Most of these models rely on strong (15) or numerous (16-18) inputs and amplification of small perturbations, leading to chaotic network dynamics and noisy single neu...

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“…Studies using electrical microstimulation of local sites in different areas of visual cortex (16) and somatosensory cortex (17) of non-human primates have shown that activation of neurons with relatively low currents is readily detected. Whether neuronal activity in the FEF can be reported has not been answered.…”

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confidence: 99%

Electrical microstimulation thresholds for behavioral detection and saccades in monkey frontal eye fields

Murphey

Maunsell

2008

Proc. Natl. Acad. Sci. U.S.A.

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The frontal eye field (FEF) is involved in the transformation of visual signals into saccadic eye movements. Although it is often considered an oculomotor structure, several lines of evidence suggest that the FEF also contributes to visual perception and attention. To better understand the range of behaviors to which the FEF can contribute, we tested whether monkeys could detect activation of their FEF by electrical microstimulation with currents below those that cause eye movements. We found that stimulation of FEF neurons could almost always be detected at levels below those needed to generate saccades and that the electrical current needed for detection was highly correlated with that needed to generate a saccade. This relationship between detection and saccade thresholds can be explained if FEF neurons represent preparation to make particular saccades and subjects can be aware of such preparations without acting on them when the representation is not strong.T he primate frontal eye field (FEF) plays a well established role in the generation of saccades. Single-unit recordings have shown that many neurons in the FEF are active around the time of saccades of specific magnitude and direction and that a topographic representation of saccade vectors exists across the FEF (1). Electrical microstimulation of sites in the FEF can produce saccades of a particular vector (2). Ablating the FEF causes pronounced deficits in generating eye movements to visual targets (3). In humans, functional MRI studies have shown activity in the FEF is correlated with visually guided saccade generation (4), and transcranial magnetic stimulation (TMS) of the FEF has been shown to disrupt saccade generation (5, 6).Although the FEF is important in oculomotor control, several lines of evidence suggest that it plays a role that goes beyond the initiation and control of eye movements (7). The FEF receives visual inputs from the thalamus and shows extensive reciprocal connectivity with visual cortical areas (1). Single-unit recordings have shown that a substantial fraction of FEF neurons have little or no perisaccadic activity and instead have strong, short-latency visual responses (2). These visually driven neurons can respond selectivity to different stimulus dimensions (8, 9) and distinguish the behavioral relevance of stimuli in an array (10). The activity of these neurons, unlike FEF neurons with perisaccadic activity, is strongly correlated with stimulus onset and only weakly correlated with the timing of saccadic responses (11). Additionally, experiments using electrical microstimulation and TMS of the FEF have shown that FEF activation can produce effects that appear similar to spatial attention (7,(12)(13)(14)(15).To further explore the range of behaviors to which FEF activity can contribute, we have examined whether subjects can detect the activity of FEF neurons at levels that are too low to produce eye movements. Studies using electrical microstimulation of local sites in different areas of visual cortex (16) and somatosensory co...

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Behavioral Detection of Electrical Microstimulation in Different Cortical Visual Areas

Cited by 106 publications

References 48 publications

Behavioral Detectability of Single-Cell Stimulation in the Ventral Posterior Medial Nucleus of the Thalamus

Behavioral Detectability of Single-Cell Stimulation in the Ventral Posterior Medial Nucleus of the Thalamus

Cortical neural populations can guide behavior by integrating inputs linearly, independent of synchrony

Electrical microstimulation thresholds for behavioral detection and saccades in monkey frontal eye fields

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