Emergence of functional and structural properties of the head direction system by optimization of recurrent neural networks
Recent work suggests goal-driven training of neural networks can be used to model neural activity in the brain. While response properties of neurons in artificial neural networks bear similarities to those in the brain, the network architectures are often constrained to be different. Here we ask if a neural network can recover both neural representations and, if the architecture is unconstrained and optimized, the anatomical properties of neural circuits. We demonstrate this in a system where the connectivity and the functional organization have been characterized, namely, the head direction circuits of the rodent and fruit fly. We trained recurrent neural networks (RNNs) to estimate head direction through integration of angular velocity. We found that the two distinct classes of neurons observed in the head direction system, the Ring neurons and the Shifter neurons, emerged naturally in artificial neural networks as a result of training. Furthermore, connectivity analysis and in-silico neurophysiology revealed structural and mechanistic similarities between artificial networks and the head direction system. Overall, our results show that optimization of RNNs in a goal-driven task can recapitulate the structure and function of biological circuits, suggesting that artificial neural networks can be used to study the brain at the level of both neural activity and anatomical organization.
Artificial neural networks have been increasingly used to study biological neural circuits. In particular, recent work in vision demonstrated that convolutional neural networks (CNNs) trained to perform visual object classification provide state-of-the-art models that match neural responses along various stages of visual processing (Yamins et al., 2014; Khaligh-Razavi and Kriegeskorte, 2014; Yamins and DiCarlo, 2016; Cadieu et al., 2014; Güçlü and van Gerven, 2015; Kriegeskorte, 2015). Recurrent neural networks (RNNs) trained on cognitive tasks have also been used to account for neural response characteristics in various domains (Mante et al., 2013; Sussillo et al., 2015; Song et al., 2016; Cueva and Wei, 2018; Banino et al., 2018; Remington et al., 2018; Wang et al., 2018; Orhan and Ma, 2019; Yang et al., 2019). While these results provide important insights on how information is processed in neural circuits, it is unclear whether artificial neural networks have converged upon similar architectures as the brain to perform either visual or cognitive tasks. Answering this question requires understanding the functional, structural, and mechanistic properties of artificial neural networks and of relevant neural circuits.
We address these challenges using the brain’s internal compass - the head direction system, a system that has accumulated substantial amounts of functional and structural data over the past few decades in rodents and fruit flies (Taube et al., 1990a, b; Turner-Evans et al., 2017; Green et al., 2017; Seelig and Jayaraman, 2015; Stone et al., 2017; Lin et al., 2013; Finkelstein et al., 2015; Wolff et al., 2015; Green and Maimon, 2018). We trained RNNs to perform a simple angular velocity (AV) integration task (Etienne and Jeffery, 2004) and asked whether the anatomical and functional features that have emerged as a result of stochastic gradient descent bear similarities to biological networks sculpted by long evolutionary time. By leveraging existing knowledge of the biological head direction (HD) systems, we demonstrate that RNNs exhibit striking similarities in both structure and function. Our results suggest that goal-driven training of artificial neural networks provide a framework to study neural systems at the level of both neural activity and anatomical organization.
2.1 Model structure
We trained our networks to estimate the agent’s current head direction by integrating angular velocity over time (Fig. 1f). Our network model consists of a set of recurrently connected units (), which are initialized to be randomly connected, with no self-connections allowed during training. The dynamics of each unit in the network is governed by the standard continuous-time RNN equation:
for . The firing rate of each unit, , is related to its total input through a rectified nonlinearity, . Every unit in the RNN receives input from all other units through the recurrent weight matrix and also receives external input, , through the weight matrix . These weight matrices are randomly initialized so no structure is a priori introduced into the network. Each unit has an associated bias, which is learned and an associated noise term, , sampled at every timestep from a Gaussian with zero mean and constant variance. The network was simulated using the Euler method for timesteps of duration ( is set to be 250ms throughout the paper).
Let be the current head direction. Input to the RNN is composed of three terms: two inputs encode the initial head direction in the form of and , and a scalar input encodes both clockwise (CW, negative) and counterclockwise, (CCW, positive) angular velocity at every timestep. The RNN is connected to two linear readout neurons, and , which are trained to track current head direction in the form of and . The activities of and are given by:
2.2 Input statistics
Velocity at every timestep (assumed to be 25 ms) is sampled from a zero-inflated Gaussian distribution (see Fig. 5). Momentum is incorporated for smooth movement trajectories, consistent with the observed animal behavior in flies and rodents. More specifically, we updated the angular velocity as AV() = + momentumAV(), where is a zero mean Gaussian random variable with standard deviation of one. In the Main condition, we set radians/timestep and the momentum to be 0.8, corresponding to a mean absolute AV of 100 deg/s. These parameters are set to roughly match the angular velocity distribution of the rat and fly (Stackman and Taube, 1998; Sharp et al., 2001; Bender and Dickinson, 2006; Raudies and Hasselmo, 2012). In Sec. 4, we manipulate the magnitude of AV by changing to see how the trained RNN may solve the integration task differently.
We optimized the network parameters , , and to minimize the mean-squared error in equation (3) between the target head direction and the network outputs generated according to equation (2), plus a metabolic cost for large firing rates ( regularization on ).
3 Functional and structural properties emerged in the network
We found that the trained network could accurately track the angular velocity (Fig. 1g). We first examined the functional and structural properties of model units in the trained RNN and compared them to the experimental data from the head direction system in rodents and flies.
3.1 Emergence of HD cells (Ring units) and HD AV cells (shifters)
Emergence of different classes of neurons with distinct tuning properties
We first plotted the neural activity of each unit as a function of HD and AV (Fig. 2a). This revealed two distinct classes of units based on the strength of their HD and AV tuning (see Appendix Fig. 6a,b,c). Units with essentially zero activity are excluded from further analyses. The first class of neurons exhibited HD tuning with minimal AV tuning (Fig. 2f). The second class of neurons were tuned to both HD and AV and can be further subdivided into two populations - one with high firing rate when animal performs CCW rotation (positive AV), the other favoring CW rotation (negative AV) (CW tuned cell shown in Fig. 2g). Moreover, the preferred head direction of each sub-population of neurons tile the complete angular space (Fig. 2b). Embedding the model units into 3D space using t-SNE reveals a clear ring-like structure, with the three classes of units being separated (Fig. 2c).
Mapping the functional architecture of RNN to neurophysiology
Neurons with HD tuning but not AV tuning have been widely reported in rodents (Taube et al., 1990a; Blair and Sharp, 1995; Stackman and Taube, 1998), although the HD*AV tuning profiles of neurons are rarely shown (but see Lozano et al. (2017)). By re-analyzing the data from Peyrache et al. (2015), we find that neurons in the anterodorsal thalamic nucleus (ADN) of the rat brain are selectively tuned to HD but not AV (Fig. 2d, also see Lozano et al. (2017)), with HD*AV tuning profile similar to what our model predicts. Preliminary evidence suggests that this might also be true for ellipsoid body (EB) ring neurons in the fruit fly HD system (Green et al., 2017; Turner-Evans et al., 2017).
Neurons tuned to both HD and AV tuning have also been reported previously in rodents and fruit flies (Sharp et al., 2001; Stackman and Taube, 1998; Bassett and Taube, 2001), although the joint HD*AV tuning profiles of neurons have only been documented anecdotally with a few cells (Turner-Evans et al. (2017)). In rodents, certain cells are also observed to display HD and AV tuning (Fig. 2e). In addition, in the fruit fly heading system, neurons on the two sides of the protocerebral bridge (PB) (Pfeiffer and Homberg, 2014) are also tuned to CW and CCW rotation, respectively, and tile the complete angular space, much like what has been observed in our trained network (Green et al., 2017; Turner-Evans et al., 2017). These observations collectively suggest that neurons that are HD but not AV selective in our model can be tentatively mapped to “Ring” units in the EB, and the two sub-populations of neurons tuned to both HD and AV map to “Shifter” neurons on the left PB and right PB, respectively. We will correspondingly refer to our model neurons as either ‘Ring’ units or ‘CW/CCW Shifters’(Further justification of the terminology will be given in Sec. 3.2 & 3.3).
Tuning properties of model neurons match experimental data
We next sought to examine the tuning properties of both Ring units and Shifters of our network in greater detail. First, we observe that for both Ring units and Shifters, the HD tuning curve varies as a function of AV (see example Ring unit in Fig. 2f and example Shifter in Fig. 2g). Population summary statistics concerning the amount of tuning shift are shown in Appendix Fig. 7a. The preferred HD tuning is biased towards a more CW angle at CW angular velocities, and vice versa for CCW angular velocities. Consistent with this observation, the HD tuning curves in rodents were also dependent upon AV (see example neurons in Fig. 2h,i) (Blair and Sharp, 1995; Stackman and Taube, 1998; Taube and Muller, 1998; Blair et al., 1997, 1998). Second, the AV tuning curves for the Shifters exhibit graded response profiles, consistent with the measured AV tuning curves in flies and rodents (see Fig. 1b,d). Across neurons, the angular velocity tuning curves show substantial diversity (see Appendix Fig. 6b), also consistent with experimental reports (Turner-Evans et al., 2017).
In summary, the majority of units in the trained RNN could be mapped onto the biological head direction system in both general functional architecture and also in detailed tuning properties. Our model unifies a diverse set of experimental observations, suggesting that these neural response properties are the consequence of a network solving an angular integration task optimally.
3.2 Connectivity structure of the network
Previous experiments have detailed a subset of connections between EB and PB neurons in the fruit fly. We next analyzed the connectivity of Ring units and Shifters in the trained RNN to ask whether it recapitulates these connectivity patterns - a test which has never been done to our knowledge in any system between artificial and biological neural networks (see Fig. 3).
Ring units exhibit local excitation and long-range inhibition
We ordered Ring units, CCW Shifters, and CW Shifters by their preferred head direction tuning and plotted their connection strengths (Fig. 3a). This revealed highly structured connectivity patterns within and between each class of units. We first focused on the connections between individual Ring units and observed a pattern of local excitation and global inhibition. Neurons that have similar preferred head directions are connected through positive weights and neurons whose preferred head directions are anti-phase are connected through negative weights (Fig. 3b). This pattern is consistent with the connectivity patterns inferred in recent work based on detailed calcium imaging and optogenetic perturbation experiments (Kim et al., 2017), with one caveat that the connectivity pattern inferred in this study is based on the effective connectivity rather than anatomical connectivity. We conjecture that Ring units in the trained RNN serve to maintain a stable activity bump in the absence of inputs (see section 3.3), as proposed in previous theoretical models (Turing, 1952; Amari, 1977; Zhang, 1996).
Asymmetric connectivity from Shifters to Ring units
We then analyzed the connectivity between Ring units and Shifters. We found that CW shifters excite Ring units with preferred head directions that are clockwise to its own, and inhibit Ring units with preferred head directions counterclockwise to its own (Fig. 3b). The opposite pattern is observed for CCW shifters. Such asymmetric connections from Shifters to the Ring units are consistent with the connectivity pattern observed between the PB and the EB in the fruit fly central complex (Lin et al., 2013; Green et al., 2017; Turner-Evans et al., 2017), and also in agreement with previously proposed mechanisms of angular integration (Skaggs et al., 1995; Green et al., 2017; Turner-Evans et al., 2017; Zhang, 1996) (Fig. 3b). We note that while the connectivity between PB Shifters and EB Ring units are one-to-one (Lin et al., 2013; Wolff et al., 2015; Green et al., 2017), the connectivity profile in our model is broad, with a single CW Shifter exciting multiple Ring units with preferred HDs that are clockwise to its own, and vice versa for CCW shifters.
In summary, the RNN developed several anatomical features that are consistent with structures reported or hypothesized in previous experimental results. A few novel predictions are worth mentioning. First, in our model the connectivity between CW and CCW Shifters exhibit specific recurrent connectivity (Fig. 8). Second, the connections from Shifters to Ring units exhibit not only excitation in the direction of heading motion, but also inhibition that is lagging in the opposite direction. This inhibitory connection has not been observed in experiments yet but may facilitate the rotation of the neural bump in the ring units during turning (Wolff et al., 2015; Franconville et al., 2018; Green et al., 2017; Green and Maimon, 2018). In the future, EM reconstructions together with functional imaging and optogenetics should allow direct tests of these predictions.
3.3 Probing the computation in the network
We have segregated neurons into Ring and Shifter populations according to their HD and AV tuning, and have shown that they exhibit different connectivity patterns that are suggestive of different functions. Ring units putatively maintain the current heading direction and shifter units putatively rotate activity on the ring according to the direction of angular velocity. To substantiate these functional properties, we performed a series of perturbation experiments by lesioning specific subsets of connections.
Perturbation while holding a constant head direction
We first lesioned connections when there is zero angular velocity input. Normally, the network maintains a stable bump of activity within each class of neurons, i.e., Ring units, CW Shifters, and CCW Shifters (see Fig. 4a,b). We first lesioned connections from Ring units to all units and found that the activity bumps in all three classes disappeared and were replaced by diffuse activity in a large proportion of units. As a consequence, the network could not report an accurate estimate of its current heading direction. Furthermore, when the connections were restored, a bump formed again without any external input (Fig. 4d), suggesting the network can spontaneously generate an activity bump through recurrent connections mediated by Ring units.
We then lesioned connections from CW Shifters to all units and found that all three bumps exhibit a CCW rotation, and the read-out units correspondingly reported a CCW rotation of heading direction (Fig. 4e,f). Analogous results were obtained with lesions of CCW Shifters, which resulted in a CW drifting bump of activity (Fig. 4g,h). These results are consistent with the hypothesis that CW and CCW Shifters simultaneously activate the ring, with mutually cancelling signals, even when the heading direction is stationary. When connections are lesioned from both CW and CCW Shifters to all units, we observe that Ring units are still capable of holding a stable HD activity bump (Fig. 4i,j), consistent with the predictions that while CW/CCW shifters are necessary for updating heading during motion, Ring units are responsible for maintaining heading.
Perturbation while integrating constant angular velocity
We next lesioned connections during either constant CW or CCW angular velocity. Normally, the network can integrate AV accurately (Fig. 4k-n). As expected, during CCW rotation, we observe a corresponding rotation of the activity bump in Ring units and in CCW Shifters, but CW Shifters display low levels of activity. The converse is true during CW rotation. We first lesioned connections from CW Shifters to all units, and found that it significantly impaired rotation in the CW direction, and also increased the rotation speed in the CCW direction. Lesioning of CCW Shifters to all units had the opposite effect, significantly impairing rotation in the CCW direction. These results are consistent with the hypothesis that CW/CCW Shifters are responsible for shifting the bump in a CW and CCW direction, respectively, and are consistent with the data in Green et al. (2017), which shows that inhibition of Shifter units in the PB of the fruit fly heading system impairs the integration of HD. Our lesion experiments further support the segregation of units into modular components that function to separately maintain and update heading during angular motion.
4 Adaptation of network properties to input statistics
Optimal computation requires the system to adapt to the statistical structure of the inputs (Barlow, 1961; Attneave, 1954). In order to understand how the statistical properties of the input trajectories affect how a network solves the task, we trained RNNs to integrate inputs generated from low and high AV distributions.
When networks are trained with small angular velocities, we observe the presence of more units with strong head direction tuning but minimal angular velocity tuning. Conversely, when networks are trained with large AV inputs, fewer ring units emerge and more units become Shifter-like and exhibit both HD and AV tuning (Fig. 5c,f,i). We sought to quantify the overall AV tuning under each velocity regime by computing the slope of each neuron’s AV tuning curve at its preferred HD angle. We found that by increasing the magnitude of AV inputs, more neurons developed strong AV tuning (Fig. 5b,e,h). In summary, with a slowly changing head direction trajectory, it is advantageous to allocate more resources to hold a stable activity bump, and this requires more ring units. In contrast, with quickly changing inputs, the system must rapidly update the activity bump to integrate head direction, requiring more shifter units. This prediction may be relevant for understanding the diversity of the HD systems across different animal species, as different species exhibit different overall head turning behavior depending on the ecological demand (Stone et al., 2017; Seelig and Jayaraman, 2015; Heinze, 2017; Finkelstein et al., 2018).
Previous work in the sensory systems have mainly focused on obtaining an optimal representation (Barlow, 1961; Laughlin, 1981; Linsker, 1988; Olshausen and Field, 1996; Simoncelli and Olshausen, 2001; Yamins et al., 2014; Khaligh-Razavi and Kriegeskorte, 2014) with feedforward models. Several recent studies have probed the importance of recurrent connections in understanding neural computation by training RNNs to perform tasks (e.g., Mante et al. (2013); Sussillo et al. (2015); Cueva and Wei (2018)), but the relation of these trained networks to the anatomy and function of brain circuits are not mapped. Using the head direction system, we demonstrate that goal-driven optimization of recurrent neural networks can be used to understand the functional, structural and mechanistic properties of neural circuits. While we have mainly used perturbation analysis to reveal the dynamics of the trained RNN, other methods could also be applied to analyze the network. For example, in Appendix Fig. 10, using fixed point analysis (Sussillo and Barak, 2013; Maheswaranathan et al., 2019), we found evidence consistent with attractor dynamics. Due to the limited amount of experimental data available, comparisons regarding tuning properties and connectivity are largely qualitative. In the future, studies of the relevant brain areas using Neuropixel probes (Jun et al., 2017) and calcium imaging (Denk et al., 1990) will provide a more in-depth characterization of the properties of HD circuits, and will facilitate a more quantitative comparison between model and experiment.
In the current work, we did not impose any additional structural constraint on the RNNs during training. We have chosen to do so in order to see what structural properties would emerge as a consequence of optimizing the network to solve the task. It is interesting to consider how additional structural constraints affect the representation and computation in the trained RNNs. One possibility would to be to have the input or output units only connect to a subset of the RNN units. Another possibility would be to freeze a subset of connections during training. Future work should systematically explore these issues.
Recent work suggests it is possible to obtain tuning properties in RNNs with random connections (Sederberg and Nemenman, 2019). We found that training was necessary for the joint HD*AV tuning (see Appendix Fig. 9) to emerge. While Sederberg and Nemenman (2019) consider a simple binary classification task, our integration task is computationally more complicated. Stable HD tuning requires the system to keep track of HD by accurate integration of AV, and to stably store these values over time. This computation might be difficult for a random network to perform (Cueva et al., 2019).
Our approach contrasts with previous network models for the HD system, which are based on hand-crafted connectivity (Zhang, 1996; Skaggs et al., 1995; Xie et al., 2002; Green et al., 2017; Kim et al., 2017; Knierim and Zhang, 2012; Song and Wang, 2005; Su et al., 2017; Stone et al., 2017). Our modeling approach optimizes for task performance through stochastic gradient descent. We found that different input statistics lead to different heading representations in an RNN, suggesting that the optimal architecture of a neural network varies depending on the task demand - an insight that would be difficult to obtain using the traditional approach of hand-crafting network solutions. Although we have focused on a simple integration task, this framework should be of general relevance to other neural systems as well, providing a new approach to understand neural computation at multiple levels.
Our model may be used as a building block for AI systems to perform general navigation (Pei et al., 2019). In order to effectively navigate in complex environments, the agent would need to construct a cognitive map of the surrounding environment and update its own position during motion. A circuit that performs heading integration will likely be combined with another circuit to integrate the magnitude of motion (speed) to perform dead reckoning. Training RNNs to perform more challenging navigation tasks such as these, along with multiple sources of inputs, i.e., vestibular, visual, auditory, will be useful for building robust navigational systems and for improving our understanding of the computational mechanisms of navigation in the brain (Cueva and Wei, 2018; Banino et al., 2018).
Research supported by NSF NeuroNex Award DBI-1707398 and the Gatsby Charitable Foundation. We would like to thank Kenneth Kay for careful reading of an earlier version of the paper, and Rong Zhu for helping preparing panel d in Figure 2.
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