Abstract
In the brain, networks of neurons produce activity that is decoded into perceptions and actions. How the dynamics of neural networks support this decoding is a major scientific question. That is, while we understand the basic mechanisms by which neurons produce activity in the form of spikes, whether these dynamics reflect an overlying functional objective is not understood. In this paper, we examine neuronal dynamics from a first-principles control-theoretic viewpoint. Specifically, we postulate an objective wherein neuronal spiking activity is decoded into a control signal that subsequently drives a linear system. Then, using a recently proposed principle from theoretical neuroscience, we optimize the production of spikes so that the linear system in question achieves reference tracking. It turns out that such optimization leads to a recurrent network architecture wherein each neuron possess integrative dynamics. The network amounts to an efficient, distributed event-based controller where each neuron (node) produces a spike if doing so improves tracking performance. Moreover, the dynamics provide inherent robustness properties, so that if some neurons fail, others will compensate by increasing their activity so that the tracking objective is met.
Similar content being viewed by others
References
Todorov E, Jordan MI (2002) Optimal feedback control as a theory of motor coordination. Nat Neurosci 5(11):1226–1235
Paul JW (1989) Neural networks for control and system identification. In: Proceedings of the 28th IEEE conference on decision and control, 1989. IEEE, pp 260–265
Narendra KS, Parthasarathy K (1990) Identification and control of dynamical systems using neural networks. IEEE Trans Neural Netw 1(1):4–27
Eliasmith C, Anderson CH (2004) Neural engineering: computation, representation, and dynamics in neurobiological systems. MIT press, Cambridge
Hunt KJ, Sbarbaro D, Zbikowski R, Gawthrop PJ (1992) Neural networks for control systems—a survey. Automatica 28(6):1083–1112
Miller WT, Werbos PJ, Sutton RS (1995) Neural networks for control. MIT press, Cambridge
Lewis FW, Jagannathan S, Yesildirak A (1998) Neural network control of robot manipulators and non-linear systems. CRC Press, Boca Raton
Lukoševičius M, Jaeger H (2009) Reservoir computing approaches to recurrent neural network training. Comput Sci Rev 3(3):127–149
Bialek W, Rieke F, Van Steveninck De Ruyter RR, Warland D (1991) Reading a neural code. Science 252(5014):1854–1857
Abbott LF, DePasquale B, Memmesheimer R-M (2016) Building functional networks of spiking model neurons. Nat Neurosci 19(3):350–355
Rao RPN, Ballard DH (1999) Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat Neurosci 2(1):79
Bastos AM, Usrey WM, Adams RA, Mangun GR, Fries P, Friston KJ (2012) Canonical microcircuits for predictive coding. Neuron 76(4):695–711
Boerlin M, Denève S (2011) Spike-based population coding and working memory. PLoS Comput Biol 7(2):e1001080
Martin B, Christian KM, Sophie D (2013) Predictive coding of dynamical variables in balanced spiking networks. PLoS Comput Biol 9(11):e1003258
Fuqiang H, James R, ShiNung C (2017) Optimizing the dynamics of spiking networks for decoding and control. In: American control conference (ACC), 2017. IEEE, pp 2792–2798
Abbott LF (1999) Lapicque’s introduction of the integrate-and-fire model neuron (1907). Brain Res Bull 50(5–6):303–304
Bekolay T, Bergstra J, Hunsberger E, DeWolf T, Stewart TC, Rasmussen D, Choo X, Voelker A, Eliasmith C (2014) Nengo: a python tool for building large-scale functional brain models. Front Neuroinf 7:48
Waegeman T, Schrauwen B et al (2012) Feedback control by online learning an inverse model. IEEE Trans Neural Netw Learn Syst 23(10):1637–1648
Olfati-Saber R, Fax JA, Murray RM (2007) Consensus and cooperation in networked multi-agent systems. Proc IEEE 95(1):215–233
Seuret A, Prieur C, Tarbouriech S, Zaccarian L (2016) Lq-based event-triggered controller co-design for saturated linear systems. Automatica 74:47–54
Peter D, Abbott LF (2001) Theoretical neuroscience, vol 10. MIT Press, Cambridge
Kalman RE (1963) Mathematical description of linear dynamical systems. J Soc Ind Appl Math Ser A Control 1(2):152–192
Johnson EC, Jones DL, Ratnam R (2016) A minimum-error, energy-constrained neural code is an instantaneous-rate code. J Comput Neurosci 40(2):193–206
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Rodolphe Sepulchre.
ShiNung Ching holds a Career Award at the Scientific Interface from the Burroughs-Wellcome Fund. This work was partially supported by AFOSR 15RT0189, NSF ECCS 1509342 and NSF CMMI 1537015, from the US Air Force Office of Scientific Research and the US National Science Foundation, respectively.
This article belongs to the Special Issue on Control Theory in Biology and Medicine. It derived from a workshop at the Mathematical Biosciences Institute, Ohio State University, Columbus, OH, USA.
A Derivation of the spiking rule (6)–(12)
A Derivation of the spiking rule (6)–(12)
The methodology to derive the dynamics of the spiking network is based on the schema originally developed in [14]. Our derivation deviates insofar as we utilize the feedback error directly, consistent with our considering of a control rather than prediction objective.
We begin by quantifying the effect of any added spike on the overall cost. Assume that the kth neuron is silent at time \(t_{s}\) and there are no spikes since time \(t_{s}\), then we can get the expression
where \(\tilde{r}(t)\) denotes the firing rate at time t assuming no spikes fired since time \(t_{s}\).
If the kth neuron spikes at time \(t_{s}\), then a delta function \(\delta (t-t_{s})\) is added to \(o_{k}(t)\) resulting in
Define \(\tilde{u}(t)\) and \(\tilde{x}(t) = {\text {e}}^{A(t-t_{s})}x(t_{s}) + \int _{t_{s}}^{t}{\text {e}}^{A(t-\tau )}B\tilde{u}(\tau )\mathrm {d}\tau \) as the decoded output and the system states when there is no spike since time \(t_{s}\), then according to the relationship between u(t) and r(t), o(t), i.e., Eq. (3), we have
where \(\varGamma _{k}\) is the kth column of \(\varGamma \) while \(\varOmega _{k}\) is the kth column of \(\varOmega \). Similarly, by Eq. (2), we obtain
In summary, when there is a new spike from the kth neuron at time \(t_{s}\), the firing rate, decoded output and system states have sudden changes as
where
where \(\mathbf {1}(t)\) denotes the unit Heaviside function. For convenience, from this point afterward, we will use h and H to denote \(h(t-t_{s})\) and \(H(t-t_{s})\), respectively.
With the above equations, the spiking assumption (5) can be translated into
With the definitions of \(\ell _1\) and \(\ell _2\) norms , we get
Note that \(h(\tau -t_{s}) = {\text {e}}^{-\lambda _{d}(\tau -t_{s})}= 0\) and \({\text {e}}^{A(\tau -t_{s})}=0 \) for \(\tau < t_{s}\), and rearrange the inequality to obtain
By examining \(\epsilon \ll \lambda _{d}\) into the future, we can then approximate the integrands as constants so that (using \(h(\tau -t_{s})\approx 1\), \(H(\tau -t_{s})\approx 0\) and \({\text {e}}^{A(\tau -t_{s})}\approx I\) for \(\tau -t_{s} \sim \epsilon \))
Defining
the spiking rule becomes
This implies that when \(v_{k}(t)\) is larger than \(\bar{v}_{k}\), the kth neuron fires a spike, thus decreasing the value of the cost function.
It now remains to deduce the differential form of the dynamics on the latent variable \(v_k(t)\). With \(V = (v_{1},\ldots ,v_{N})\), we can write
Let \(e(t) = \hat{x}(t)- x(t)\) and take derivatives of Eq. (25), we could get that
Note that \(u(t) = \frac{1}{\lambda _d}\varGamma r(t)+\varOmega o(t)\), and
then,
This last step highlights the core difference in the network dynamics under the control objective versus the original predictive coding framework. Because \(\dot{\hat{x}}\) and \(\dot{x}\) are both subject to the same (linear) dynamics in our case, the feedback error \((\hat{x} - x)\) can be retained explicitly here.
With the definition in (11) and (12), the voltage differential equation can be finally written as
Rights and permissions
About this article
Cite this article
Huang, F., Ching, S. Spiking networks as efficient distributed controllers. Biol Cybern 113, 179–190 (2019). https://doi.org/10.1007/s00422-018-0769-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00422-018-0769-7