Vertebrate brain theory

ISBN 978-3-00-064888-5

Monograph of Dr. rer. nat. Andreas Heinrich Malczan

3.19      The development of the olfactory system

The olfactory system represented the top floor in the rope ladder system. Both the sensory input core, the motor output core and all mean value cores were arranged in this one plane and were located close together. Later, when the individual modalities unfolded into separate modality loops, the olfactory system remained within the temporal loop, because it was now a very conservative, evolutionarily ancient structure that could not produce its own modality loop. It remained at the top of the temporal loop as the topmost level. Later, with the spatial extension of all cortical loops, it remained an independent component of the developing temporal lobe of the vertebrate brain. Its various substructures formed a complex called the amygdala. Later, the hippocampus formed as a new structure.

Within this olfactory system different nuclei were formed in the course of evolution, which are described below.

Theorem of the lateral amygdala as input nucleus  

The lateral amygdala (basal nucleus) is the sensory centre of the olfactory floor in the early rope ladder system and receives both the input of the olfactory receptors and the signals from the floors below rising in the rope ladder system. It forms the input core of the olfactory floor.

Theorem of the basal, parvocellular amygdala as initial nucleus

The parvocellular part of the basal nucleus of the amygdala is the motor centre of the olfactory level in the early rope ladder system and sends the output in descending order to the lower levels, so that ultimately the motor neurons can be activated via the nucleus ruber. It is the output nucleus of the olfactory floor. Its neurons correspond to the class 5 neurons of the cortex.

This motor centre of the rope ladder system also projects into the different mean value cores of the olfactory floor and the lower floors, in particular also into the dopaminergic mean value centre, which in turn causes a back projection.

Theorem of the basal magnocellular amygdala

The glutamatergic mean centre of the olfactory floor is formed by the magnocellular neurons of the basal nucleus. This nucleus is functionally comparable to the subthalamic nucleus below the thalamic level after splitting the modalities into separate turning loops.

Theorem of the septum as cholinergic mean nucleus

The septum forms the cholinergic mean center of the olfactory floor in the early stranded wire system and sends the output to both the amygdala and deeper substructures. The cholinergic mean centre of the other different modalities is formed by the nucleus basalis Meynert.

The first disadvantage of the developing olfactory sense was the transience of the olfactory signals. As soon as the scents, which also spread in the primordial ocean, were no longer perceptible, the olfactory receptors stopped firing. The rapid diffusion ensured that the scent cloud of prey or predators quickly disappeared. Then there was no longer an olfactory signal that could activate the motor system.

One way to extend the duration of the olfactory signals was to repeat these signals. The olfactory signals from the receptors arrived via their axons in the first segment of the early rope ladder nervous system, where they activated the class 3 commissure neurons of the sensory center. Today they are called granule cells and projected via commissure axons into the motor centre, which formed the basal (parvocellular) amygdala. These axons are now called moss fibers. The action potentials generated on the moss fibres spread relatively slowly.

These unmyelinated axons, the moss fibres, have been tapped in the course of evolution by many newly formed echoneurons, which we can regard as offshoots of class 3 neurons. And because a single synapse could not transmit the necessary excitation at all, hundreds of synapses formed between the moss fibres and the echoneurons, with the axons and dendrites forming highly branched, moss-like structures. The resulting increase in the number of synapses enabled the moss fibre signals to generate action potentials in the echoneurons. Thus, a sequence of action potentials was created from a single action potential. On the unmyelinated moss fibre the action potential spread relatively slowly. And whenever it passed a connected echoneuron, it also generated an action potential in the echoneuron. Initially, the echo neurons had thicker axons and therefore transmitted the action potentials at higher speed. In the course of evolution, they formed myelin sheaths, which further increased the speed at which action potentials spread. These axons are now known as Schaffer collaterals. They guided the action potentials of a moss fibre to a common integration neuron. This neuron then received the sequence of action potentials from the corresponding echo neurons of the same moss fiber. Due to the lower propagation speed along the moss fiber, however, these arrived at the integration neuron with a time delay. An olfactory action potential generated a sequence of successive action potentials in this structure. And since each output neuron of the olfactory sense was supplied to its own moss fiber, the associated integration neuron generated a sequence of action potentials in response to a single action potential in case of activity. The duration of this action potential sequence makes it possible to prolong a motor response to the olfactory signal. This structure was formed in the olfactory cortex and is called the hippocampus. In parallel to its formation, the associated spatial demand caused the topmost, i.e. the olfactory level of the rope ladder nervous system to expand. The associated ventricular space became larger as a result.

Figure: Echogenerator (principle circuit diagram) - Source: A. H. Malczan

 

Echoerzeugung auf Verzögerungsleitungen im Hippocampus

Figure 19 - Echo generation on delay lines in the hippocampus

The hippocampus prolonged the ability to respond to olfactory signals by converting each action potential into a longer sequence of action potentials. Its output reached the amygdala, which projected into the motor neurons. In the course of evolution, an excitatory back projection from the amygdala to the hippocampus developed, which was a point-to-point projection. Each granule cell received exactly the amygdala output that it had produced as amygdala input. This resulted in positive feedback, which in turn created a rotational memory for olfactory signals.

Theorem of echo formation in the hippocampus

The olfactory receptor signals of the cortex led to the excitation of granule cells in the hippocampus. Each action potential of a granule cell propagated on its unmyelinated axon at a slower rate and, as it propagated, also generated an action potential in each echoneuron of the CA3 region. The action potentials of the echoneurons arrived with a certain time delay in a common output neuron of the CA1 region via the initially thicker Schaffer collaterals, which were even myelinated in the course of evolution. Thus, an action potential of a granule cell was transformed into a sequence of action potentials in the corresponding output neuron of the CA1 region. This corresponded to a frequency multiplication of the fire rate of the input.

The output of the hippocampus was generated by frequency multiplication from the original olfactory receptor output and therefore generated much stronger and longer lasting motor responses.

Here, of course, the question arises at which evolutionary time the Schaffer collateral in the hippocampus could form a (albeit weak) myelin sheath. This was necessary to perfect the described function.

Grundschaltung Hippocampus als Echogenerator

Figure 20 - Hippocampus basic circuit as echo generator

We often encounter feedback in neuronal structures. The feedback of hippocampal signals back to the hippocampus created a long-term memory. This required a neuron nucleus that received the hippocampal signals and sent them back to the hippocampus. This nucleus was the amygdala. The amygdala was an output structure of the olfactory level of the segmented bilateria whose line led to the vertebrates.

Theorem of the amygdala as feedback and output structure of the olfactory system

The signals of the hippocampus reached the amygdala, which, on the one hand, as an output nucleus, activated the motor connective neurons of class 5, which projected to the motor neurons of the head region and trunk. On the other hand, the amygdala projected via commissure neurons of class 3 to the input neurons of the hippocampus, so that there was a positive feedback.

Theorem of the formation of inhibitory interneurons in the hippocampus and amygdala

In the hippocampus as well as in the amygdala, inhibitory interneurons were formed, which caused lateral inhibition and thus led to contrast enhancement between weak and strong signals.

Theorem of the exciting projection of the hippocampus into the septum

  The output of the hippocampus reaches the septum, which serves as the mean center of the olfactory floor.

Each mean value system projects back into the original system. The hippocampus, however, was tionally excited by the frequency multiplication of the olfactory input and the positive feedback to the amygdala. Exciting feedback of the septal signals would not have been beneficial. Therefore, the septum with its excitatory transmitter projected acetylcholine into the inhibitory interneurons of the hippocampus, thereby temporarily stopping its excitation. As a result, it no longer received any hippocampal signals itself, so that its output was lost. However, since the hippocampus still received excitatory amygdala signals, its tonic excitation began again. Thus, each brief phase of tonic excitation of the hippocampus was followed by a phase of total inhibition. This oscillation form of the hippocampus is called hippocampal theta. The inhibitory interneurons, which caused lateral inhibition, led to the synchronization of this oscillation form among the many output neurons.

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Figure 21 - The hippocampal theta

Theorem of the origin of the hippocampal theta

The hippocampal theta is caused by the positive feedback of the hippocampal oscillation via the amygdala and the negative feedback via the septum.

Here, the transit time of the signals from the hippocampus to the amygdala and back to the hippocampus as well as the transit time of the signals from the hippocampus to the septum and back to the hippocampus plays a major role. However, the frequency of the oscillation is limited upwards by the refractory time of the neurons involved. A loss of the septal projection has dramatic consequences.

Theorem of the development of epileptic seizures

The cessation of the periodic inhibition of tonic excitation in the hippocampus caused by the septum via interneurons leads to pathological excitation states in the hippocampal system, which become apparent as epileptic seizures.

In the course of evolutionary development, the amygdala received not only olfactory signals but also signals from other modalities, including visual ones. These signals rose from the tectum in a headward direction and reached the amygdala via the ascending projecting class 4 connective neurons and the horizontal class 3 commissive neurons.

In the amygdala itself, a separate mean value centre developed and formed an independent core, which is called the basal amygdala.

An olfactory signal - later also a signal of another modality - which found an input into the hippocampal system, rotated permanently in the feedback loop between hippocampus and amygdala. This corresponded to long-term memory, and the rotating signa could, for example, trigger motor reactions as an output of the amygdala. Thus, a short-term olfactory signal could be used to start a prey search that would last forever due to the signal rotation. However, the latter was not appropriate. The search had to be aborted at some point. This was only possible if there were structures that generated an abort signal that inhibited the signal rotation. In this case a time-controlled interruption of rotation was favourable. For example after 1 hour, maybe even after 2 hours, but at the latest when a new day started, the search was stopped and everything was set to start. For this purpose, time-controlled nuclei were used, such as the nucleus suprachiasmaticus. This nucleus in the ventral hypothalamus is used for circadian control and was suitable to emit a time signal to inhibit the hippocampal rotations. The interruption of the rotation took place in inhibitory neurons of the amygdala, which received the excitatory stop signal and in turn inhibited the amygdalaneurons. These neurons later formed the central amygdala, which, however, was to perform further tasks in the course of evolution.

Theorem of the interruption of the hippocampal continuous rotation

The inhibitory neurons, which received stop signals and thus interrupted the continuous hippocampal rotation of signals, formed the central core of the amygdala. They emerged from the inhibitory interneurons, which were used in the amygdala for lateral inhibition and thus for contrast enhancement. Later, the central nucleus took over further tasks.

Monograph of Dr. rer. nat. Andreas Heinrich Malczan