# Odor recognition and segmentation by coupled olfactory bulb and cortical networks

## 1 Introduction

There is a great deal of current interest in how neural systems, both artificial and natural, can use top-down feedback to modulate input processing. Here we propose a minimal model for an olfactory system in which feedback enables it to perform an essential task – olfactory segmentation. Most olfactory systems need to detect, recognize, and segment odor objects. Segmentation is necessary because different odors give overlapping activity patterns on odor receptor neurons, of which there are hundreds of types BuckAxel , and each has a broad spectrum of response to different odor molecules Shepherd90 . Different odor objects seldom enter the environment in the same sniff cycle, but they often stay together in the environment afterwards. Humans usually can not identify the individual odor objects in mixtures Moncrieff , although they easily perceive an incoming odor superposed on pre-existing ones. Our model performs odor segmentation temporally: First one odor is detected and encoded by the olfactory bulb and recognized by the associative memory circuits of the olfactory cortex. Then the cortex gives an odor-specific feedback to the bulb to inhibit the response or adapt to this odor, so that a superposed second odor arriving later can be detected and recognized with undiminished sensitivity while the sensitivity to the pre-existing odor is reduced, as observed psychophysically Moncrieff . The stimulus-specific feedback makes odor adaptation an intelligent computational strategy, unlike simple fatigue, which is not sufficient for odor segmentation. Our model displays the oscillatory neural activities in the bulb and cortex as observed physiologically FS . Furthermore, odor cross-adaptation — the suppression and distortion of odor perception immediately after an exposure to another odor — as observed psychophysically Moncrieff , is a consequence of this model.

## 2 The Model

Our model (Fig. 1) describes the essential elements of primary olfactory neural circuitry: the olfactory bulb, the olfactory cortex, and feedforward and feedback coupling between them. The formal neurons in our system model the collective activity of local populations of real neurons. The synaptic architecture is consistent with the known physiology and anatomy of the olfactory system in most mammalian species Shepherd7990 .

Our bulb model contains interacting excitatory mitral and inhibitory granule cells, with membrane potentials $`x_i`$ and $`y_i`$ respectively, and firing rates $`g_x(x_i)`$ and $`g_y(y_i)`$ respectively (see LH  and Li90  for details). The odor input $`I_i`$ drives the dynamics   
$`\dot{x}_i=\alpha x_i_jH_{ij}^0g_y(y_j)+I_i\dot{y}_i=\alpha y_j+_jW_{ij}^0g_x(x_j)+I_i^c,`$   
where $`\alpha x_i`$ and $`\alpha y_i`$ model the decays to resting potentials, $`𝖧_{ij}^0>0`$ and $`𝖶_{ij}^0>0`$ the synaptic connections from the granule to mitral cells and vice versa, and vector $`𝐈^c`$ (components $`I_i^c`$) the feedback signal from the cortex to the granule cells. Slowly varying input $`𝐈`$ and $`𝐈^c`$ adiabatically determine the fixed or equilibrium point $`\overline{𝐱}`$ and $`\overline{𝐲}`$ of the equations. Neural activities oscillates around this equilibrium as $`𝐱=\overline{𝐱}+_kc_k𝐗_ke^{\alpha t\pm \mathrm{i}(\sqrt{\lambda }_kt+\varphi _k)}`$, where $`𝐗_k`$ is an eigenvector of $`𝖠=\mathrm{𝖧𝖶}`$ with eigenvalue $`\lambda _k`$, and $`H_{ij}=H_{ij}^0g_y^{}(\overline{y}_j)`$ and $`W_{ij}=W_{ij}^0g_x^{}(\overline{x}_j)`$. Spontaneous oscillation occurs if $`\mathrm{Re}(\alpha \pm i\sqrt{\lambda }_k)>0`$; then the fastest-growing mode, call it $`𝐗_1`$, dominates the output and the entire bulb oscillates with a single frequency $`\omega _1\mathrm{Re}(\sqrt{\lambda _1})`$, and the oscillation amplitudes and phases is approximately the complex vector $`X_1`$. Thus, the bulb encodes the input via the steps: (1) the input $`𝐈`$ determines $`(\overline{𝐱},\overline{𝐲})`$, which in turn (2) determines the matrix $`𝖠`$, which then (3) determines whether the bulb will give spontanous oscillatory outputs and, if it does, the oscillation pattern $`𝐗_1`$ and frequency $`\omega _1`$.

The mitral cell outputs $`g_x(x_i)`$ are transformed to an effective input $`I_i^b`$ to the excitatory (pyramidal) cells of the cortex by (1) a convergent-divergent bulbar-cortex connection matrix and (2) an effective high-pass filtering via feedforward interneurons in the cortex. Our cortical model is structurally similar to that of the bulb. We focus only on the upper layer pyramidal cells and feedback interneurons:   
$`\dot{u}_i=\alpha u_i\beta ^0g_v(v_i)+_jJ_{ij}^0g_u(u_j)+I_i^b,\dot{v}_i=\alpha v_i+\gamma ^0g_u(u_i)+_j\stackrel{~}{W}_{ij}^0g_u(u_j)`$,   
where $`𝐮`$, $`𝐯`$, and $`\stackrel{~}{𝖶}^0`$ correspond to $`𝐱`$, $`𝐲`$, and $`𝖶^0`$ for the bulb. $`𝖩^0`$ is global excitatory-to-excitatory connections, $`\beta ^0`$ and $`\gamma ^0`$ are local synaptic couplings.

Carrying out the same kind of linearization around the fixed point $`(\overline{𝐮},\overline{𝐯})`$ as in the bulb, we obtain a system of driven coupled oscillators. With appropriate cell nonlinearities and overall scale of the synaptic connections, the system does not oscillate spontaneously, nor does it respond much to random or irrelevant inputs. However, the cortex will resonate vigorously when the driving oscillatory force $`𝐈^b`$ matches one of intrinsic oscillatory modes $`\stackrel{}{\xi }^\mu `$ in frequency and patterns amplitudes and phases. These intrinsic modes $`\stackrel{}{\xi }^\mu `$ for $`\mu =1,2,\mathrm{}P`$, are memory items in an associative memory system Haberly85 ; WB92 ; AGL , and can be stored in the synapses $`𝖩^0`$ and $`\stackrel{~}{𝖶}^0`$ in a generalized Hebb-Hopfield fashion

$`J_{ij}^0\frac{\mathrm{i}}{\omega }(\beta \stackrel{~}{W}_{ij}^0\alpha J_{ij}^0)=J_\mu \xi _i^\mu \xi _j^\mu /g_u^{}(\overline{u}_j).`$

Fig. 2 shows that 3 odors A, B, and C all evoke bulbar oscillatory responses. However only odor A and B are stored in the in the cortical synapses; hence the cortical oscillatory response to odor C is almost nonexistent.

It was shown in Li90  that a suitable DC feedback signal to suppress the odor-specific activity in the bulb is $`d𝐈^c=𝖧^1\alpha d𝐈`$. Somehow, this feedback should be constructed from the cortical outputs that contains the odor information. We do not know how this is done in cortical circuitry, so we treat this part of the problem phenomenologically. First, we transform the AC signal in the pyramidal cell output $`g_u(u_i)`$ to a slow DC like signal by thresholding $`g_u(u_i)`$ and then passing it through two successive very slow leaky integrators. One can then easily construct a synaptic connection matrix to transform this signal to the desired feedback signal for the odor input that evoked the cortical output $`g_u(u)`$ in the past sniffs.

Feedback signal slowly builds up and the adaptation to odor A becomes effective at the second sniff (Fig. 3A), and the system responds to odor A+B at the third sniff in a way as if only odor B were present (Fig. 3B), achieving odor adaptation and segmentation consistent with human behavior. Quantitative analysis confirms that the response to the segmented odor B in the third sniff is about 98% similar to that of response to odor B alone. Simulations show that odor adaptation eventually achieves an equilibrium level when insignificant residual responses to background odors maintain a steady feedback signal. A consequence of the model is olfactory cross-adaptation, when the background odor A is suddenly removed and odor B is presented. The feedback signal or background adaptation to odor A persists for a while and significantly distorts (and suppresses) the response to, and thus the percept of, odor B (Fig. (3C)), as observed psychophysically Moncrieff .

## 3 Discussion

We have augmented the bulb model developed in earlier work by one of us LH ; Li90  with a model of the pyriform cortex and with feedforward and feedback connections between it and the bulb. It is a minimal computational model for how an olfactory system can detect, recognize and segment odors. As far as we know, this is the simplest system consistent with anatomical knowledge that can perform these three tasks, all of which are fundamental for olfaction. Our model does not deal with other computational tasks, such as hierachical catagorization of odors AGL .

The resonant associative memory recognition mechanism and the slow feedback to the granule (inhibitory) neurons of the bulb are essential parts of our model, but many of the details of the present treatment are not. For example, the slow feedback signal could be implemented by many other mechanisms, but it must be slow. These essential features are necessary in order that the model be consistent with the observed phenomenology of the olfactory system.