The neurochemical changes underlying human emotions and social behavior are largely unknown. Here we report on the changes in the levels of two hypothalamic neuropeptides, hypocretin-1 (Hcrt-1) and melanin concentrating hormone (MCH), measured in the human amygdala. We show that Hcrt-1 levels are maximal during positive emotion, social interaction, and anger, behaviors that induce cataplexy in human narcoleptics. In contrast, MCH levels are minimal during social interaction, but are increased after eating. Both peptides are at minimal levels during periods of postoperative pain despite high levels of arousal. MCH levels increase at sleep onset, consistent with a role in sleep induction, whereas Hcrt-1 levels increase at wake onset, consistent with a role in wake induction. Levels of these two peptides in humans are not simply linked to arousal, but rather to specific emotions and state transitions. Other arousal systems may be similarly emotionally specialized.
Episodic memory, which depends critically on the integrity of the medial temporal lobe (MTL), has been described as “mental time travel” in which the rememberer “jumps back in time.” The neural mechanism underlying this ability remains elusive. Mathematical and computational models of performance in episodic memory tasks provide a specific hypothesis regarding the computation that supports such a jump back in time. The models suggest that a representation of temporal context, a representation that changes gradually over macroscopic periods of time, is the cue for episodic recall. According to these models, a jump back in time corresponds to a stimulus recovering a prior state of temporal context. In vivo single-neuron recordings were taken from the human MTL while epilepsy patients distinguished novel from repeated images in a continuous recognition memory task. The firing pattern of the ensemble of MTL neurons showed robust temporal autocorrelation over macroscopic periods of time during performance of the memory task. The gradually-changing part of the ensemble state was causally affected by the visual stimulus being presented. Critically, repetition of a stimulus caused the ensemble to elicit a pattern of activity that resembled the pattern of activity present before the initial presentation of the stimulus. These findings confirm a direct prediction of this class of temporal context models and may be a signature of the mechanism that underlies the experience of episodic memory as mental time travel.
The P300 speller is a system designed to restore communication to patients with advanced neuromuscular disorders. This study was designed to explore the potential improvement from using electrocorticography (ECoG) compared to the more traditional usage of electroencephalography (EEG).
We tested the P300 speller on two epilepsy patients with temporary subdural electrode arrays over the occipital and temporal lobes respectively. We then performed offline analysis to determine the accuracy and bit rate of the system and integrated spectral features into the classifier and used a natural language processing (NLP) algorithm to further improve the results.
The subject with the occipital grid achieved an accuracy of 82.77% and a bit rate of 41.02, which improved to 96.31% and 49.47 respectively using a language model and spectral features. The temporal grid patient achieved an accuracy of 59.03% and a bit rate of 18.26 with an improvement to 75.81% and 27.05 respectively using a language model and spectral features. Spatial analysis of the individual electrodes showed best performance using signals generated and recorded near the occipital pole.
Using ECoG and integrating language information and spectral features can improve the bit rate of a P300 speller system. This improvement is sensitive to the electrode placement and likely depends on visually evoked potentials.
This study shows that there can be an improvement in BCI performance when using ECoG, but that it is sensitive to the electrode location.
brain-computer interface; electrocorticography; event-related potential; P300; speller; natural language processing
Recording the activity of neurons is a mainstay of animal memory research, while human recordings are generally limited to the activity of large ensembles of cells. The relationship between ensemble activity and neural firing rate during declarative memory processes, however, remains unclear. We recorded neurons and local field potentials (LFPs) simultaneously from the same sites in the human hippocampus and entorhinal cortex (ERC) in patients with implanted intracranial electrodes during a virtual taxi-driver task that also included a memory retrieval component. Neurons increased their firing rate in response to specific passengers or landmarks both during navigation and retrieval. Although we did not find item specificity in the broadband LFP, both θ- and γ-band LFPs increased power to specific items on a small but significant percent of channels. These responses, however, did not correlate with item-specific neural responses. To contrast item-specific responses with process-specific responses during memory, we compared neural and LFP responses during encoding (navigation) and retrieval (associative and item-specific recognition). A subset of neurons also altered firing rates nonspecifically while subjects viewed items during encoding. Interestingly, LFPs in the hippocampus and ERC increased in power nonspecifically while subjects viewed items during retrieval, more often during associative than item-recognition. Furthermore, we found no correlation between neural firing rate and broadband, θ-band, and γ-band LFPs during process-specific responses. Our findings suggest that neuronal firing and ensemble activity can be dissociated during encoding, item-maintenance, and retrieval in the human hippocampal area, likely relating to functional properties unique to this region.
hippocampus; depth electrode; local field potentials; single neuron; human memory; declarative memory
Patient studies have not provided consistent evidence for interictal neuronal hyperexcitability inside the seizure onset zone (SOZ). We hypothesized that gray matter (GM) loss could have important effects on neuronal firing, and quantifying these effects would reveal significant differences in neuronal firing inside versus outside the SOZ.
MRI and computational unfolding of mesial temporal lobe (MTL) subregions was used to construct anatomical maps to compute GM loss in presurgical patients with medically intractable focal seizures in relation to control subjects. In patients, these same maps were used to locate the position of microelectrodes that recorded interictal neuronal activity. Single neuron firing and burst rates were evaluated in relation to GM loss and MTL subregions inside and outside the SOZ.
MTL GM thickness was reduced inside and outside the SOZ in patients with respect to control subjects, yet GM loss was associated more strongly with firing and burst rates in several MTL subregions inside the SOZ. Adjusting single neuron firing and burst rates for the effects of GM loss revealed significantly higher firing rates in the subregion consisting of dentate gyrus and CA2 and CA3 (CA23DG), as well as CA1 and entorhinal cortex (EC) inside versus outside the SOZ where normalized MRI GM loss was ≥1.40 mm. Firing rates were higher in subicular cortex inside the SOZ at GM loss ≥1.97 mm, while burst rates were higher in CA23DG, CA1, and EC inside than outside the SOZ at similar levels of GM loss.
The correlation between GM loss and increased firing and burst rates suggests GM structural alterations in MTL subregions are associated with interictal neuronal hyperexcitability inside the SOZ. Significant differences in firing rates and bursting in areas with GM loss inside compared to outside the SOZ indicate that synaptic reorganization following cell loss could be associated with varying degrees of epileptogenicity in patients with intractable focal seizures.
epilepsy; atrophy; interictal; hippocampus; MRI; microelectrode; single neuron
The amygdala is important in emotion, but it remains unknown whether it is specialized for certain stimulus categories. We analyzed responses recorded from 489 single neurons in the amygdalae of 41 neurosurgical patients and found a categorical selectivity for pictures of animals in the right amygdala. This selectivity appeared to be independent of emotional valence or arousal and may reflect the importance that animals held throughout our evolutionary past.
The medial temporal structures, including the hippocampus and the entorhinal cortex, are critical for the ability to transform daily experience into lasting memories. We tested the hypothesis that deep-brain stimulation of the hippocampus or entorhinal cortex alters memory performance.
We implanted intracranial depth electrodes in seven subjects to identify seizure-onset zones for subsequent epilepsy surgery. The subjects completed a spatial learning task during which they learned destinations within virtual environments. During half the learning trials, focal electrical stimulation was given below the threshold that elicits an afterdischarge (i.e., a neuronal discharge that occurs after termination of the stimulus).
Entorhinal stimulation applied while the subjects learned locations of landmarks enhanced their subsequent memory of these locations: the subjects reached these landmarks more quickly and by shorter routes, as compared with locations learned without stimulation. Entorhinal stimulation also resulted in a resetting of the phase of the theta rhythm, as shown on the hippocampal electroencephalogram. Direct hippocampal stimulation was not effective. In this small series, no adverse events associated with the procedure were observed.
Stimulation of the entorhinal region enhanced memory of spatial information when applied during learning. (Funded by the National Institutes of Health and the Dana Foundation.)
Sleep spindles are an electroencephalographic (EEG) hallmark of non-rapid eye movement (NREM) sleep and are believed to mediate many sleep-related functions, from memory consolidation to cortical development. Spindles differ in location, frequency, and association with slow waves, but whether this heterogeneity may reflect different physiological processes and potentially serve different functional roles remains unclear. Here we utilized a unique opportunity to record intracranial depth EEG and single-unit activity in multiple brain regions of neurosurgical patients to better characterize spindle activity in human sleep. We find that spindles occur across multiple neocortical regions, and less frequently also in the parahippocampal gyrus and hippocampus. Most spindles are spatially restricted to specific brain regions. In addition, spindle frequency is topographically organized with a sharp transition around the supplementary motor area between fast (13-15Hz) centroparietal spindles often occurring with slow wave up-states, and slow (9-12Hz) frontal spindles occurring 200ms later on average. Spindle variability across regions may reflect the underlying thalamocortical projections. We also find that during individual spindles, frequency decreases within and between regions. In addition, deeper sleep is associated with a reduction in spindle occurrence and spindle frequency. Frequency changes between regions, during individual spindles, and across sleep may reflect the same phenomenon, the underlying level of thalamocortical hyperpolarization. Finally, during spindles neuronal firing rates are not consistently modulated, although some neurons exhibit phase-locked discharges. Overall, anatomical considerations can account well for regional spindle characteristics, while variable hyperpolarization levels can explain differences in spindle frequency.
The most prominent EEG events in sleep are slow waves, reflecting a slow (<1 Hz) oscillation between up and down states in cortical neurons. It is unknown whether slow oscillations are synchronous across the majority or the minority of brain regions—are they a global or local phenomenon? To examine this, we recorded simultaneously scalp EEG, intracerebral EEG, and unit firing in multiple brain regions of neurosurgical patients. We find that most sleep slow waves and the underlying active and inactive neuronal states occur locally. Thus, especially in late sleep, some regions can be active while others are silent. We also find that slow waves can propagate, usually from medial prefrontal cortex to the medial temporal lobe and hippocampus. Sleep spindles, the other hallmark of NREM sleep EEG, are likewise predominantly local. Thus, intracerebral communication during sleep is constrained because slow and spindle oscillations often occur out-of-phase in different brain regions.
There is compelling evidence that pathological high frequency oscillations (HFOs) called Fast Ripples (FR, 150–500 Hz) reflect abnormal synchronous neuronal discharges in areas responsible for seizure genesis in patients with mesial temporal lobe epilepsy (MTLE). It is hypothesized that morphological changes associated with hippocampal atrophy (HA) contribute to the generation of FR, yet there is limited evidence that hippocampal FR-generating sites correspond with local areas of atrophy.
Interictal HFOs were recorded from hippocampal microelectrodes in ten patients with MTLE. Rates of FR and Ripple discharge from each microelectrode were evaluated in relation to local measures of HA obtained using 3D MRI hippocampal modeling.
Rates of FR discharge were three times higher in areas of significant local HA compared to rates in non-atrophic areas. Furthermore, FR occurrence correlated directly with the severity of damage in these local atrophic regions. In contrast, we found no difference in rates of Ripple discharge between local atrophic and non-atrophic areas.
The proximity between local HA and microelectrode-recorded FR suggest morphological changes such as neuron loss and synaptic reorganization may contribute to the generation of FR. Pathological HFOs, such as FR, may provide a reliable surrogate marker of abnormal neuronal excitability in hippocampal areas responsible for the generation of spontaneous seizures in patients with MTLE. Based on these data, it is possible that MRI-based measures of local HA could identify FR-generating regions, and thus provide a non-invasive means to localize epileptogenic regions in hippocampus.
Understanding how self-initiated behavior is encoded by neuronal circuits in the human brain remains elusive. We recorded the activity of 1019 neurons while twelve subjects performed self-initiated finger movement. We report progressive neuronal recruitment over ~1500 ms before subjects report making the decision to move. We observed progressive increase or decrease in neuronal firing rate, particularly in the supplementary motor area (SMA), as the reported time of decision was approached. A population of 256 SMA neurons is sufficient to predict in single trials the impending decision to move with accuracy greater than 80% already 700 ms prior to subjects’ awareness. Furthermore, we predict, with a precision of a few hundred ms, the actual time point of this voluntary decision to move. We implement a computational model whereby volition emerges once a change in internally generated firing rate of neuronal assemblies crosses a threshold.
Actions are often internally guided, reflecting our covert will and intentions. The dorsomedial prefrontal cortex, including the pre-Supplementary Motor Area (pre-SMA), has been implicated in the internally generated aspects of action planning, such as choice and intention. Yet, the mechanism by which this area interacts with other cognitive brain regions such as the dorsolateral prefrontal cortex, a central node in decision-making, is still unclear. To shed light on this mechanism, brain activity was measured via fMRI and intracranial EEG in two studies during the performance of visually cued repeated finger tapping in which the choice of finger was guided by either a presented number (external) or self-choice (internal). A functional-MRI (fMRI) study in 15 healthy participants demonstrated that the pre-SMA, compared to the SMA proper, was more active and also more functionally correlated with the dorsolateral prefrontal cortex during internally compared to externally guided action planning (p < 0.05, random effect). In a similar manner, an intracranial-EEG study in five epilepsy patients showed greater inter-regional gamma-related connectivity between electrodes situated in medial and lateral aspects of the prefrontal cortex for internally compared to externally guided actions. Although this finding was observed for groups of electrodes situated both in the pre-SMA and SMA-proper, increased intra-cluster gamma-related connectivity was only observed for the pre-SMA (sign-test, p < 0.0001). Overall our findings provide multi-scale indications for the involvement of the dorsomedial prefrontal cortex, and especially the pre-SMA, in generating internally guided motor planning. Our intracranial-EEG results further point to enhanced functional connectivity between decision-making- and motor planning aspects of the PFC, as a possible neural mechanism for internally generated action planning.
fMRI; iEEG; gamma band; internally guided; prefrontal cortex; finger tapping
The effect of stimulus modulation rate on the underlying neural activity in human auditory cortex is not clear. Human studies (using both invasive and noninvasive techniques) have demonstrated that at the population level, auditory cortex follows stimulus envelope. Here we examined the effect of stimulus modulation rate by using a rare opportunity to record both spiking activity and local field potentials (LFP) in auditory cortex of patients during repeated presentations of an audio-visual movie clip presented at normal, double, and quadruple speeds. Mean firing rate during evoked activity remained the same across speeds and the temporal response profile of firing rate modulations at increased stimulus speeds was a linearly scaled version of the response during slower speeds. Additionally, stimulus induced power modulation of local field potentials in the high gamma band (64–128 Hz) exhibited similar temporal scaling as the neuronal firing rate modulations. Our data confirm and extend previous studies in humans and anesthetized animals, supporting a model in which both firing rate, and high-gamma LFP power modulations in auditory cortex follow the temporal envelope of the stimulus across different modulation rates.
human; auditory cortex; spiking activity; local field potentials (LFP)
Different pictures of Marilyn Monroe can evoke the same percept, even if greatly modified as in Andy Warhol’s famous portraits. But how does the brain recognize highly variable pictures as the same percept? Various studies have provided insights into how visual information is processed along the “ventral pathway,” via both single-cell recordings in monkeys [1, 2] and functional imaging in humans [3, 4]. Interestingly, in humans, the same “concept” of Marilyn Monroe can be evoked with other stimulus modalities, for instance by hearing or reading her name. Brain imaging studies have identified cortical areas selective to voices [5, 6] and visual word forms [7, 8]. However, how visual, text, and sound information can elicit a unique percept is still largely unknown. By using presentations of pictures and of spoken and written names, we show that (1) single neurons in the human medial temporal lobe (MTL) respond selectively to representations of the same individual across different sensory modalities; (2) the degree of multimodal invariance increases along the hierarchical structure within the MTL; and (3) such neuronal representations can be generated within less than a day or two. These results demonstrate that single neurons can encode percepts in an explicit, selective, and invariant manner, even if evoked by different sensory modalities.
Daily life continually confronts us with an exuberance of external, sensory stimuli competing with a rich stream of internal deliberations, plans and ruminations. The brain must select one or more of these for further processing. How this competition is resolved across multiple sensory and cognitive regions is not known; nor is it clear how internal thoughts and attention regulate this competition1–4. Recording from single neurons in patients implanted with intracranial electrodes for clinical reasons5–9, here we demonstrate that humans can regulate the activity of their neurons in the medial temporal lobe (MTL) to alter the outcome of the contest between external images and their internal representation. Subjects looked at a hybrid superposition of two images representing familiar individuals, landmarks, objects or animals and had to enhance one image at the expense of the other, competing one. Simultaneously, the spiking activity of their MTL neurons in different subregions and hemispheres was decoded in real time to control the content of the hybrid. Subjects reliably regulated, often on the first trial, the firing rate of their neurons, increasing the rate of some while simultaneously decreasing the rate of others. They did so by focusing onto one image, which gradually became clearer on the computer screen in front of their eyes, and thereby overriding sensory input. On the basis of the firing of these MTL neurons, the dynamics of the competition between visual images in the subject's mind was visualized on an external display.
A fundamental question in neuroscience concerns the relation between the spiking of individual neurons and the aggregate electrical activity of neuronal ensembles as seen in local-field potentials (LFPs). Because LFPs reflect both spiking activity and subthreshold events, this question is not simply one of data aggregation. Recording from 20 neurosurgical patients, we directly examined the relation between LFPs and neuronal spiking. Examining 2,030 neurons in widespread brain regions, we found that firing rates were positively correlated with broadband (2 – 150 Hz) shifts in the LFP power spectrum. In contrast, narrowband oscillations correlated both positively and negatively with firing rates at different recording sites. Broadband power shifts were a more-reliable predictor of neuronal spiking than narrowband power shifts. These findings suggest that broadband LFP power provides valuable information concerning neuronal activity beyond that contained in narrowband oscillations.
Local field potentials; Broadband; Oscillations; Single-units; Humans; Epilepsy
During spatial navigation, lesion and functional imaging studies suggest that the right hemisphere has a unique functional role. However, studies of direct human brain recordings have not reported interhemisphere differences in navigation-related oscillatory activity. We investigated this apparent discrepancy using intracranial electroencephalographic recordings from 24 neurosurgical patients playing a virtual taxi driver game. When patients were virtually moving in the game, brain oscillations at various frequencies increased in amplitude compared with periods of virtual stillness. Using log-linear analysis, we analyzed the region and frequency specificities of this pattern and found that neocortical movement-related gamma oscillations (34–54 Hz) were significantly lateralized to the right hemisphere, especially in posterior neocortex. We also observed a similar right lateralization of gamma oscillations related to searching for objects at unknown virtual locations. Thus, our results indicate that gamma oscillations in the right neocortex play a special role in human spatial navigation.
Human recognition performance is characterized by abrupt changes in perceptual states. Understanding the neuronal dynamics underlying such transitions could provide important insights into mechanisms of recognition and perceptual awareness. Here we examined patients monitored for clinical purposes with multiple subdural electrodes. The patients participated in a backward masking experiment in which pictures of various object categories were presented briefly followed by a mask. We recorded ECoG from 445 electrodes placed in 11 patients. We found a striking increase in gamma power (30–70 Hz) and evoked responses specifically associated with successful recognition. The enhanced activation occurred 150–200 ms after stimulus onset and consistently outlasted the stimulus presentation. We propose that the gamma and evoked potential activations reflect a rapid increase in recurrent neuronal activity that plays a critical role in the emergence of a recognizable visual percept in conscious awareness.
While automatic spike sorting has been investigated for decades, little attention has been allotted to consistent evaluation criteria that will automatically determine whether a cluster of spikes represents the activity of a single cell or a multiunit. Consequently, the main tool for evaluation has remained visual inspection by a human. This paper quantifies the visual inspection process. The results are well-defined criteria for evaluation, which are mainly based on visual features of the spike waveform, and an automatic adaptive algorithm that learns the classification by a given human and can apply similar visual characteristics for classification of new data. To evaluate the suggested criteria, we recorded the activity of 1652 units (single cells and multiunits) from the cerebrum of 12 human patients undergoing evaluation for epilepsy surgery requiring implantation of chronic intracranial depth electrodes. The proposed method performed similar to human classifiers and obtained significantly higher accuracy than two existing methods (three variants of each). Evaluation on two synthetic datasets is also provided. The criteria are suggested as a standard for evaluation of the quality of separation that will allow comparison between different studies. The proposed algorithm is suitable for real-time operation and as such may allow brain–computer interfaces to treat single cells differently than multiunits.
The supplementary motor area (SMA) plays an important role in planning, initiation, and execution of motor acts. Patients with SMA lesions are impaired in various kinematic parameters, such as velocity and duration of movement. However, the relationships between neuronal activity and these parameters in the human brain have not been fully characterized. This is a study of single-neuron activity during a continuous volitional motor task, with the goal of clarifying these relationships for SMA neurons and other frontal lobe regions in humans.
The participants were 7 patients undergoing evaluation for epilepsy surgery requiring implantation of intracranial depth electrodes. Single-unit recordings were conducted while the patients played a computer game involving movement of a cursor in a simple maze.
In the SMA proper, most of the recorded units exhibited a monotonic relationship between the unit firing rate and hand motion speed. The vast majority of SMA proper units with this property showed an inverse relation, that is, firing rate decrease with speed increase. In addition, most of the SMA proper units were selective to the direction of hand motion. These relationships were far less frequent in the pre-SMA, anterior cingulate gyrus, and orbitofrontal cortex.
The findings suggest that the SMA proper takes part in the control of kinematic parameters of end-effector motion, and thus lend support to the idea of connecting neuroprosthetic devices to the human SMA.
brain-computer interface; electrophysiological study; human single unit; motor control; movement speed; supplementary motor area
Neurons in the temporal lobe of both monkeys and humans show selective responses to classes of visual stimuli and even to specific individuals. In this study, we investigate the latency and selectivity of visually responsive neurons recorded from microelectrodes in the parahippocampal cortex, entorhinal cortex, hippocampus, and amygdala of human subjects during a visual object presentation task. During 96 experimental sessions in 35 subjects, we recorded from a total of 3278 neurons. Of these units, 398 responded selectively to one or more of the presented stimuli. Mean response latencies were substantially larger than those reported in monkeys. We observed a highly significant correlation between the latency and the selectivity of these neurons: the longer the latency the greater the selectivity. Particularly, parahippocampal neurons were found to respond significantly earlier and less selectively than those in the other three regions. Regional analysis showed significant correlations between latency and selectivity within the parahippocampal cortex, entorhinal cortex, and hippocampus, but not within the amygdala. The later and more selective responses tended to be generated by cells with sparse baseline firing rates and vice versa. Our results provide direct evidence for hierarchical processing of sensory information at the interface between the visual pathway and the limbic system, by which increasingly refined and specific representations of stimulus identity are generated over time along the anatomic pathways of the medial temporal lobe.
single-unit recordings; object recognition; parahippocampal gyrus; entorhinal cortex; hippocampus; amygdala
The emergence of memory, a trace of things past, into human consciousness is one of the greatest mysteries of the human mind. Whereas the neuronal basis of recognition memory can be probed experimentally in human and nonhuman primates, the study of free recall requires that the mind declare the occurrence of a recalled memory (an event intrinsic to the organism and invisible to an observer). Here, we report the activity of single neurons in the human hippocampus and surrounding areas when subjects first view cinematic episodes consisting of audiovisual sequences and again later when they freely recall these episodes. A subset of these neurons exhibited selective firing, which often persisted throughout and following specific episodes for as long as 12 seconds. Verbal reports of memories of these specific episodes at the time of free recall were preceded by selective reactivation of the same hippocampal and entorhinal cortex neurons. We suggest that this reactivation is an internally generated neuronal correlate for the subjective experience of spontaneous emergence of human recollection.
Animal studies have shown robust electrophysiological activity in the sensory cortex in the absence of stimuli or tasks. Similarly, recent human functional magnetic resonance imaging (fMRI) revealed widespread, spontaneously emerging cortical fluctuations. However, it is unknown what neuronal dynamics underlie this spontaneous activity in the human brain. Here we studied this issue by combining bilateral single-unit, local field potentials (LFPs) and intracranial electrocorticography (ECoG) recordings in individuals undergoing clinical monitoring. We found slow (<0.1 Hz, following 1/f-like profiles) spontaneous fluctuations of neuronal activity with significant interhemispheric correlations. These fluctuations were evident mainly in neuronal firing rates and in gamma (40–100 Hz) LFP power modulations. Notably, the interhemispheric correlations were enhanced during rapid eye movement and stage 2 sleep. Multiple intracranial ECoG recordings revealed clear selectivity for functional networks in the spontaneous gamma LFP power modulations. Our results point to slow spontaneous modulations in firing rate and gamma LFP as the likely correlates of spontaneous fMRI fluctuations in the human sensory cortex.
We demonstrate that human electrophysiological recordings of the local field potential (LFP) from intracranial electrodes, acquired from a variety of cerebral regions, show a ubiquitous 1/f2 scaling within the power spectrum. We develop a quantitative model that treats the generation of these fields in an analogous way to that of electronic shot noise, and use this model to specifically address the cause of this 1/f2 Brownian noise. The model gives way to two analytically tractable solutions, both displaying Brownian noise: 1) uncorrelated cells that display sharp initial activity, whose extracellular fields slowly decay in time and 2) rapidly firing, temporally correlated cells that generate UP-DOWN states.