Dual Process for Intentional and Reactive Decisions

Efficient cognitive decisions should be adjustable to incoming novel information. However, most current models of decision making have so far neglected any potential interaction between intentional and stimulus-driven decisions. We report here behavioral results and a new model on the interaction between a perceptual decision and non-predictable novel information. We asked participants to anticipate their response to an external stimulus and presented this stimulus with variable delay. Participants were clearly able to adjust their initial decision to the new stimulus if this latter appeared sufficiently early. To account for these results, we present a two-stage model in which two systems, an intentional and a stimulus-driven, interact only in the second stage. In the first stage of the model, the intentional and stimulus-driven processes race independently to reach a transition threshold between the two stages. The model can also account for results of a second experiment where a response bias is introduced. Our model is consistent with some physiological results that indicate that both parallel and interactive processing take place between intentional and stimulus-driven information. It emphasizes that in natural conditions, both types of processing are important and it helps pinpoint the transition between parallel and interactive processing.     

Traveling Waves and the Processing of Weakly Tuned Inputs in a Cortical Network Module

Recent studies have shown that local cortical feedback can havean important effect on the response of neurons in primary visualcortex to the orientation of visual stimuli. In this work, westudy the role of the cortical feedback in shaping thespatiotemporal patterns of activity in cortex. Two questionsare addressed: one, what are the limitations on the ability ofcortical neurons to lock their activity to rotatingoriented stimuli within a single receptive field? Two, can thelocal architecture of visual cortex lead to the generation ofspontaneous traveling pulses of activity? We study theseissues analytically by a population-dynamic model of ahypercolumn in visual cortex. The order parameter thatdescribes the macroscopic behavior of the network is thetime-dependent population vector of the network. We firststudy the network dynamics under the influence of a weakly tunedinput that slowly rotates within the receptive field. We showthat if the cortical interactions have strong spatialmodulation, the network generates a sharply tuned activityprofile that propagates across the hypercolumn in a path thatis completely locked to the stimulus rotation. The resultantrotating population vector maintains a constant angular lagrelative to the stimulus, the magnitude of which grows with thestimulus rotation frequency. Beyond a critical frequency thepopulation vector does not lock to the stimulus but executes aquasi-periodic motion with an average frequency that is smallerthan that of the stimulus. In the second part we consider thestable intrinsic state of the cortex under the influence of isotropic stimulation. We show that if the local inhibitoryfeedback is sufficiently strong, the network does not settleinto a stationary state but develops spontaneous travelingpulses of activity. Unlike recent models of wave propagation incortical networks, the connectivity pattern in our model isspatially symmetric, hence the direction of propagation ofthese waves is arbitrary. The interaction of these waves withan external-oriented stimulus is studied. It is shown that thesystem can lock to a weakly tuned rotating stimulus if thestimulus frequency is close to the frequency of the intrinsic wave.     

Male bill colour and competition in zebra finches

Several studies have assessed the role of bill colour in sexual selection and especially with respect to sexual preferences. Even though there are indications that bill colour is related to male quality, so far it has not been shown that bill colour influences male-male interaction. We used male zebra finches with artificially coloured bills in a competitive context to measure the effect of bill colour. In these tests the experimental bird could choose between two feeding sites, each near a stimulus bird with a different bill colour. We tested orange against red, no bird against orange/red and orange/red against green respectively. We found no difference in behaviour towards an orange compared to a red billed stimulus. However the birds spent relatively more time eating when alone compared to being close to a potential competitor. In addition, more time was spent eating than on other behaviours when the birds were close to the orange/red billed stimulus compared to the green billed stimulus. So, although no effect was found in the orange against red test, the results suggest that bill colour may play some role in male-male interaction.     

Two-category model of task allocation with application to ant societies

In many network models of interacting units such as cells or insects, the coupling coefficients between units are independent of the state of the units. Here we analyze the temporal behavior of units that can switch between two 'category' states according to rules that involve category-dependent coupling coefficients. The behaviors of the category populations resulting from the asynchronous random updating of units are first classified according to the signs of the coupling coefficients using numerical simulations. They range from isolated fixed points to lines of fixed points and stochastic attractors. These behaviors are then explained analytically using iterated function systems and birth-death jump processes. The main inspiration for our work comes from studies of non-hierarchical task allocation in, e.g., harvester ant colonies where temporal fluctuations in the numbers of ants engaged in various tasks occur as circumstances require and depend on interactions between ants. We identify interaction types that produce quick recovery from perturbations to an asymptotic behavior whose characteristics are function of the coupling coefficients between ants as well as between ants and their environment. We also compute analytically the probability density of the population numbers, and show that perturbations in our model decay twice as fast as in a model with random switching dynamics. A subset of the interaction types between ants yields intrinsic stochastic asymptotic behaviors which could account for some of the experimentally observed fluctuations. Such noisy trajectories are shown to be random walks with state-dependent biases in the 'category population' phase space. With an external stimulus, the parameters of the category-switching rules become time-dependent. Depending on the growth rate of the stimulus in comparison to its population-dependent decay rate, the dynamics may qualitatively differ from the case without stimulus. Our simple two-category model provides a framework for understanding the rich variety of behaviors in network dynamics with state-dependent coupling coefficients, and especially in task allocation processes with many tasks.     

A model of naturalistic decision making in preference tests

Decisions as to whether to continue with an ongoing activity or to switch to an alternative are a constant in an animal’s natural world, and in particular underlie foraging behavior and performance in food preference tests. Stimuli experienced by the animal both impact the choice and are themselves impacted by the choice, in a dynamic back and forth. Here, we present model neural circuits, based on spiking neurons, in which the choice to switch away from ongoing behavior instantiates this back and forth, arising as a state transition in neural activity. We analyze two classes of circuit, which differ in whether state transitions result from a loss of hedonic input from the stimulus (an “entice to stay” model) or from aversive stimulus-input (a “repel to leave” model). In both classes of model, we find that the mean time spent sampling a stimulus decreases with increasing value of the alternative stimulus, a fact that we linked to the inclusion of depressing synapses in our model. The competitive interaction is much greater in “entice to stay” model networks, which has qualitative features of the marginal value theorem, and thereby provides a framework for optimal foraging behavior. We offer suggestions as to how our models could be discriminatively tested through the analysis of electrophysiological and behavioral data.     

Stimulus motion propels traveling waves in binocular rivalry

State transitions in the nervous system often take shape as traveling waves, whereby one neural state is replaced by another across space in a wave-like manner. In visual perception, transitions between the two mutually exclusive percepts that alternate when the two eyes view conflicting stimuli (binocular rivalry) may also take shape as traveling waves. The properties of these waves point to a neural substrate of binocular rivalry alternations that have the hallmark signs of lower cortical areas. In a series of experiments, we show a potent interaction between traveling waves in binocular rivalry and stimulus motion. The course of the traveling wave is biased in the motion direction of the suppressed stimulus that gains dominance by means of the wave-like transition. Thus, stimulus motion may propel the traveling wave across the stimulus to the extent that the stimulus motion dictates the traveling wave's direction completely. Using a computational model, we show that a speed-dependent asymmetry in lateral inhibitory connections between retinotopically organized and motion-sensitive neurons can explain our results. We argue that such a change in suppressive connections may play a vital role in the resolution of dynamic occlusion situations.     

Sequence matters – selective adaptation in electroantennographic response to binary odour mixtures by the Colorado potato beetle

Chemically mediated behaviour of insects is often strongly affected by mixtures of odour stimuli and their temporal characteristics. Both sensory transduction and central processing of odour mixtures can give rise to several different kinds of interaction, which can influence how individual components are perceived and processed. In particular, odour mixtures have been examined in model experiments as premixed binary mixtures in comparison with pure odour stimuli. Only in few experiments, the influence of the temporal structure of odour mixtures on odour perception has been taken into account. Natural odour stimuli often have a pulsed structure and may in general be superimposed on a background of irrelevant or interfering compounds, which can fluctuate with different frequencies, depending on their source. To achieve a better representation of these natural conditions, our odour mixing experiments apply a new kind of stimulation protocol: odours were not premixed but superimposed with a specific time pattern; one odour stimulus was presented as a longer persisting background and the second stimulus was a superimposed short test signal. To gain an overview of odour interaction patterns in the Colorado potato beetle by causing adaptation of one receptor population at naturally occurring levels of concentration and time intervals, electroantennographic recordings were made on excised antennae. A matrix of 12 stimulus compounds led to 132 pairs of compounds tested, each in the role of background and test stimulus. In 64 cases, the interaction was significantly different, when the role of background and stimulus was exchanged. Interaction patterns ranging from no interference (independence) to suppression were found and assigned to four clearly distinguishable types. We discuss that the observed effects of the presentation sequence in odour mixtures may contribute to the mechanisms of olfactory pattern recognition and olfactory contrast perception by insects.     

Brain state and plasticity: an integration of the reciprocal interaction model of sleep cycle oscillation with attentional models of hippocampal function

The present paper relates the reciprocal interaction model for sleep cycle oscillation (McCarley and Hobson, ref. 29) to an attentional model of hippocampal function (Schmajuk and Moore, ref. 44). We consider mechanisms by which the interaction between gigantocellular tegmental field (FTG) cells and locus coeruleus (LC) activity proposed by the sleep cycle model may differentially modulate the information processing carried out in the hippocampus as described by the attentional model. Our fundamental assumption is that learning about the relevancy of different stimuli is proportional to the level of LC activation. If the environment becomes unpredictable during waking, the FTG and LC are activated and the LC facilitates hippocampal learning about stimulus relevancy. In a predictable situation during waking, FTG cells discharge rarely because no novelty is detected, and LC neurons are moderately active. If the predictable situation lasts, LC cells also decrease their activity, and a sleep period might start. At sleep onset, LC inhibition decreases and FTG activity is low leading to slow sleep. As FTG activity increases and LC activity reaches its low point, REM sleep starts. Because LC activity is low during REM sleep, values of stimulus relevancy remain unchanged. Since during sleep the threshold for external stimuli is high, only internally generated novel stimuli (subjectively perceived as dream mentation) may activate the LC. LC renewed inhibitory influence on the FTG ends REM sleep.     

Coding "what" and "when" in the Archer fish retina

Traditionally, the information content of the neural response is quantified using statistics of the responses relative to stimulus onset time with the assumption that the brain uses onset time to infer stimulus identity. However, stimulus onset time must also be estimated by the brain, making the utility of such an approach questionable. How can stimulus onset be estimated from the neural responses with sufficient accuracy to ensure reliable stimulus identification? We address this question using the framework of colour coding by the archer fish retinal ganglion cell. We found that stimulus identity, “what”, can be estimated from the responses of best single cells with an accuracy comparable to that of the animal''s psychophysical estimation. However, to extract this information, an accurate estimation of stimulus onset is essential. We show that stimulus onset time, “when”, can be estimated using a linear-nonlinear readout mechanism that requires the response of a population of 100 cells. Thus, stimulus onset time can be estimated using a relatively simple readout. However, large nerve cell populations are required to achieve sufficient accuracy.

Authors Summary

In our interaction with the environment we are flooded with a stream of numerous objects and events. Our brain needs to understand the nature of these complex and rich stimuli in order to react. Research has shown ways in which a ‘what’ stimulus was presented can be encoded by the neural responses. However, to understand ‘what was the nature of the stimulus’ the brain needs to know ‘when’ the stimulus was presented. Here, we investigated how the onset of visual stimulus can be signalled by the retina to higher brain regions. We used archer fish as a framework to test the notion that the answer to the question of ‘when’ something has been presented lies within the larger cell population, whereas the answer to the question of ‘what’ has been presented may be found at the single-neuron level. The utility of the archer fish as model animal stems from its remarkable ability to shoot down insects settling on the foliage above the water level, and its ability to distinguish between artificial targets. Thus, the archer fish can provide the fish equivalent of a monkey or a human that can report psychophysical decisions.     

The interaction of clozapine with the metachlorophenylpiperazine (mCPP) discriminative stimulus

The psychotropic effects of the 5-HT_2C agonist mCPP in human subjects are blocked by the atypical antipsychotic clozapine, but not by typical antipsychotics. An understanding of the mechanistic basis for the interaction of clozapine and mCPP would provide further insight into the basis for its unique therapeutic effects in humans. Drug-induced stimulus control provides an animal model for the subjective effects of psychotropic agents in humans. In the present study, the interaction of the atypical antipsychotic clozapine and the typical antipsychotic fluphenazine with the mCPP-stimulus were defined. Neither drug antagonized the stimulus effects of mCPP in vivo. In contrast, clozapine fully antagonized the mCPP-stimulated phosphoinositide turnover at the 5-HT_2C receptor in vitro. The present data indicate that the paradigm of mCPP-induced stimulus control does not facilitate the differentiation of atypical and typical antipsychotic activities.     

Apparent discontinuities in the phase-resetting response of cardiac pacemakers

Injection of a brief stimulus pulse resets the spontaneous periodic activity of a sinoatrial node cell: a stimulus delivered early in the cycle generally delays the time of occurrence of the next action potential, while the same stimulus delivered later causes an advance. We investigate resetting in two models, one with a slow upstroke velocity and the other with a fast upstroke velocity, representing central and peripheral nodal cells, respectively. We first formulate each of these models as a classic Hodgkin-Huxley type of model and then as a model representing a population of single channels. In the Hodgkin-Huxley-type model of the slow-upstroke cell the transition from delay to advance is steep but continuous. In the corresponding single-channel model, due to the channel noise then present, repeated resetting runs at a fixed stimulus timing within the transitional range of coupling intervals lead to responses that span a range of advances and delays. In contrast, in the fast-upstroke model the transition from advance to delay is very abrupt in both classes of model, as it is in experiments on some cardiac preparations ("all-or-none" depolarization). We reduce the fast-upstroke model from the original seven-dimensional system to a three-dimensional system. The abrupt transition occurs in this reduced model when a stimulus transports the state point to one side or the other of the stable manifold of the trajectory corresponding to the eigendirection associated with the smaller of two positive eigenvalues. This stable manifold is close to the slow manifold, and so canard trajectories are seen. Our results demonstrate that the resetting response is fundamentally continuous, but extremely delicate, and thus suggest one way in which one can account for experimental discontinuities in the resetting response of a nonlinear oscillator.     

A semi-empirical cell dynamics model for bone turnover under external stimulus

The normal periodic turnover of bone is referred to as remodeling. In remodeling, old or damaged bone is removed during a 'resorption' phase and new bone is formed in its place during a 'formation' phase in a sequence of events known as coupling. Resorption is preceded by an 'activation' phase in which the signal to remodel is initiated and transmitted. Remodeling is known to involve the interaction of external stimuli, bone cells, calcium and phosphate ions, and several proteins, hormones, molecules, and factors. In this study, a semi-empirical cell dynamics model for bone remodeling under external stimulus that accounts for the interaction between bone mass, bone fluid calcium, bone calcium, and all three major bone cell types, is presented. The model is formulated to mimic biological coupling by solving separately and sequentially systems of ODEs for the activation, resorption, and formation phases of bone remodeling. The charateristic time for resorption (20 days) and the amount of resorption (~0.5%) are fixed for all simulations, but the formation time at turnover is an output of the model. The model was used to investigate the effects of different types of strain stimuli on bone turnover under bone fluid calcium balance and imbalance conditions. For bone fluid calcium balance, the model predicts complete turnover after 130 days of formation under constant 1000 microstrain stimulus; after 47 days of formation under constant 2000 microstrain stimulus; after 173 days of formation under strain-free conditions, and after 80 days of formation under monotonic increasing strain stimulus from 1000 to 2000 microstrain. For bone fluid calcium imbalance, the model predicts that complete turnover occurs after 261 days of formation under constant 1000 microstrain stimulus and that turnover never occurs under strain-free conditions. These predictions were not impacted by mean dynamic input strain stimuli of 1000 and 2000 microstrain at 1 Hz and 1000 microstrain amplitude. The formation phase of remodeling lasts longer than the resorption phase, increased strain stimulus accelerates bone turnover, while absence of strain significantly delays or prevents it, and formation time for turnover under monotonic increasing strain conditions is intermediate to those for constant strain stimuli at the minimum and maximum monotonic strain levels. These results are consistent with the biology, and with Frost's mechanostat theory.     

Stimulus amplification, efficacy, and the operational model. Part I--binary complex occupancy mechanisms.

A simple function, developed to represent the stimulus produced at the n -th step of a multistep signaling sequence, is applied to the classic model of agonist-receptor interaction. The model indicates that the relative efficacy of two agonists can be easily estimated from three experimental measures: maximal response, EC50, and apparent dissociation constant. Efficacy ratios obtained in this manner appear statistically and mathematically equivalent to those estimated with null-based methods. Enhancement of both maximal response (vertical amplification) and potency (horizontal amplification) are demonstrated to result from the interaction between highly efficacious agonists and signal transduction mechanisms. Both properties, not just relative maxima, must therefore be examined when comparing relative efficacy. Three additional generalized stimulus-response models are developed and shown to be functionally equivalent. Increasing the complexity of the function used to represent stimulus amplification does not appear to alter the conclusions derived based on the simple model of stimulus amplification. Analysis of the results also reveals a close relationship between mechanistic and operational modes of drug action, and allows operational parameters to be given mechanistic interpretation.     

A generalized linear model for estimating spectrotemporal receptive fields from responses to natural sounds

In the auditory system, the stimulus-response properties of single neurons are often described in terms of the spectrotemporal receptive field (STRF), a linear kernel relating the spectrogram of the sound stimulus to the instantaneous firing rate of the neuron. Several algorithms have been used to estimate STRFs from responses to natural stimuli; these algorithms differ in their functional models, cost functions, and regularization methods. Here, we characterize the stimulus-response function of auditory neurons using a generalized linear model (GLM). In this model, each cell's input is described by: 1) a stimulus filter (STRF); and 2) a post-spike filter, which captures dependencies on the neuron's spiking history. The output of the model is given by a series of spike trains rather than instantaneous firing rate, allowing the prediction of spike train responses to novel stimuli. We fit the model by maximum penalized likelihood to the spiking activity of zebra finch auditory midbrain neurons in response to conspecific vocalizations (songs) and modulation limited (ml) noise. We compare this model to normalized reverse correlation (NRC), the traditional method for STRF estimation, in terms of predictive power and the basic tuning properties of the estimated STRFs. We find that a GLM with a sparse prior predicts novel responses to both stimulus classes significantly better than NRC. Importantly, we find that STRFs from the two models derived from the same responses can differ substantially and that GLM STRFs are more consistent between stimulus classes than NRC STRFs. These results suggest that a GLM with a sparse prior provides a more accurate characterization of spectrotemporal tuning than does the NRC method when responses to complex sounds are studied in these neurons.     

A mathematical model of spontaneous calcium(II) oscillations in astrocytes

Astrocytes exhibit oscillations and waves of Ca²⁺ ions within their cytosol and it appears that this behavior helps facilitate the astrocyte's interaction with its environment, including its neighboring neurons. Often changes in the oscillatory behavior are initiated by an external stimulus such as glutamate, recently however, it has been observed that oscillations are also initiated spontaneously. We propose here a mathematical model of how spontaneous Ca²⁺ oscillations arise in astrocytes. This model uses the calcium-induced calcium release and inositol cross-coupling mechanisms coupled with a receptor-independent method for producing inositol (1,4,5)-trisphosphate as the heart of the model. By computationally mimicking experimental constraints we have found that this model provides results that are qualitatively similar to experiment.     

Dyslexic adults can learn from repeated stimulus presentation but have difficulties in excluding external noise

We examined whether the characteristic impairments of dyslexia are due to a deficit in excluding external noise or a deficit in taking advantage of repeated stimulus presentation. We compared non-impaired adults and adults with poor reading performance on a visual letter detection task that varied two aspects: the presence or absence of background visual noise, and a small or large stimulus set. There was no interaction between group and stimulus set size, indicating that the poor readers took advantage of repeated stimulus presentation as well as the non-impaired readers. The poor readers had higher thresholds than non-impaired readers in the presence of high external noise, but not in the absence of external noise. The results support the hypothesis that an external noise exclusion deficit, not a perceptual anchoring deficit, impairs reading for adults.     

Network Redundancy Analysis of Effective Brain Networks; a Comparison of Healthy Controls and Patients with Major Depression

This study investigated electroencephalographic correlates in chronically depressed patients compared to healthy controls using intracutaneously applied electrical pain stimulus, to better understand the interaction between pain processing and depression. A close interaction between pain and depression is generally recognized although the precise mechanisms are not yet fully understood. The present study focuses on the hypothesis that effective brain connectivity in major depression patients is altered. Multifunctional interactions between brain regions represent a robust index of effective interactions within the brain, and can be quantified by network redundancy. Thus, structural network differences between 18 normal controls and 18 major depression patients before as well as during the processing of moderately painful intracutaneous electrical stimuli were investigated on the basis of network redundancy differences. In our sample, both patients and control subjects exhibit comparable network redundancies before stimulus application. Caused by the stimulus, there is a global increase of network redundancy in both groups. This increase is diminished in the group of major depression patients. We found clear differences between patients and controls during the stimulus processing, where the network redundancy in normal controls is larger in comparison to patients. The differences might be explained by the fact that major depression patients are more restricted to the affective component of the processing. The well-established biasing to affective processing might suppress the somatosensory processing resulting in a lower number of connections within the considered network. This might then lead to a reduction in network redundancy during stimulus processing.     

Relationships between hormones and aggressive behavior in green anole lizards: an analysis using structural equation modeling

We investigated the relationship between aggressive behavior and circulating androgens in the context of agonistic social interaction and examined the effect of this interaction on the androgen-aggression relationship in response to a subsequent social challenge in male Anolis carolinensis lizards. Individuals comprising an aggressive encounter group were exposed to an aggressive conspecific male for 10 min per day during a 5-day encounter period, while controls were exposed to a neutral stimulus for the same period. On the sixth day, their responses to an intruder test were observed. At intervals, individuals were sacrificed to monitor plasma androgen levels. Structural equation modeling (SEM) was used to test three a priori interaction models of the relationship between social stimulus, aggressive behavior, and androgen. Model 1 posits that exposure to a social stimulus influences androgen and aggressive behavior independently. In Model 2, a social stimulus triggers aggressive behavior, which in turn increases circulating levels of androgen. In Model 3, exposure to a social stimulus influences circulating androgen levels, which in turn triggers aggressive behavior. During the 5 days of the encounter period, circulating testosterone (T) levels of the aggressive encounter group followed the same pattern as their aggressive behavioral responses, while the control group did not show significant changes in their aggressive behavior or T level. Our SEM results supported Model 2. A means analysis showed that during the intruder test, animals with 5 days of aggressive encounters showed more aggressive responses than did control animals, while their circulating androgen levels did not differ. This further supports Model 2, suggesting that an animal's own aggressive behavior may trigger increases in levels of plasma androgen.